Evolutionary history of wild goat (Capra aegagrus) and

the goat (C. hircus) based on the analysis of

mitochondrial and nuclear DNA polymorphism:
Implications for conservation and for the origin of the
domestication
Saeid Naderi

To cite this version:

Saeid Naderi. Evolutionary history of wild goat (Capra aegagrus) and the goat (C. hircus) based on
the analysis of mitochondrial and nuclear DNA polymorphism: Implications for conservation and for
the origin of the domestication. Ecology, environment. Université Joseph-Fourier - Grenoble I, 2007.
English. �NNT : �. �tel-00312922�

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 Ecole Doctorale Chimie et Science du Vivant

THESE
Pour obtenir le grade de DOCTEUR DE L’UNIVERSITE JOSEPH FOURIER

Spécialité Biodiversité-Ecologie-Environnement

Préparée au Laboratoire d’Ecologie Alpine (LECA)

Histoire évolutive de l’Aegagre (Capra aegagrus) et de la

chèvre (C. hircus) basée sur l’analyse du polymorphisme de
l’ADN mitochondrial et nucléaire : Implications pour la
conservation et pour l’origine de la domestication

Présentée et soutenue publiquement le 11 Décembre 2007 par

Saeid Naderi

Composition du Jury

Paolo Ajmone-Marsan, Professeur Università Cattolica del S. Cuore (Italie), Rapporteur

Olivier Hanotte, Chercheur, International Livestock Research Institute. Nairobi (Kenya),
Rapporteur
François Pompanon, Maître de Conférences à l’Université Joseph Fourier, Grenoble I,
Co-Directeur de thèse
Pierre Taberlet, Directeur de recherche à l’Université Joseph Fourier, Grenoble I,
Directeur de thèse
Jean-Denis Vigne, Chercheur au Muséum National d'Histoire Naturelle, Paris; Examinateur
A l’Iran, mon cher Pays

A ma chère famille

Et tous ceux qui me sont chers

Remerciements

Je voudrais remercier les membres du jury, Monsieur le Professeur Paolo Ajmone-

Marsan et Monsieur le Docteur Olivier Hanotte pour avoir accepté d’être les rapporteurs
de ma thèse, et Messieurs les Docteurs Jean-Denis Vigne, Pierre Taberlet et François
Pompanon pour avoir accepté d’être présents pour juger mon travail.
Ce travail fait partie d’un programme de coopération Scientifique et Technique Franco-
Iranien sous l’égide du Ministère de la Science, de la Recherche et de la Technologie
Iranien et du SFERE (La Société Française d’Exportation des Ressources Educatives).

Mon travail de recherche a été effectué au sein du laboratoire d’écologie Alpine (LECA)
à Grenoble, sous la direction de M. Pierre Taberlet, Directeur de Recherche au CNRS, à
qui j’adresse ici mes sincères remerciements pour m’avoir accueilli dans son laboratoire.

Mes remerciements vont également au Ministère de la Science, de la Recherche et de la

Technologie d’Iran grâce auquel j’ai pu bénéficier d’une bourse doctorale (Numéro
800125). Un grand merci aux conseillers scientifiques d’Iran à Paris, Messieurs Rahmati
et Abdollahi, ainsi que de l’organisme SFERE, pour tout le soutien et la gentillesse qu’ils
m’ont témoigné.
Je tiens à remercier ici tous ceux qui m’ont aidé, soutenu et encouragé pendant ma thèse.
Je suis très heureux de pouvoir exprimer ma profonde gratitude envers mes directeurs de
thèse M. Pierre Taberlet, et M. François Pompanon.
Je ne sais comment remercier Pierre, de m’avoir encouragé et guidé tout au long de mon
travail, tout en m’accordant sa confiance. Il m’a inspiré mon travail et su me diriger avec
beaucoup de patience et de sympathie. J’ai pu, au cours des quatre années passées au
laboratoire apprécier non seulement sa conscience scientifique mais aussi et surtout ses
remarquables qualités humaines, qu’il trouve ici l’expression de ma profonde
reconnaissance.
J’adresse mes sincères remerciements à François, vraiment. Il a toujours été présent pour
mes questions avec sa bonne humeur et son sourire habituel. Je le remercie infiniment
pour son aide, ses conseils, ses encouragements, sa disponibilité et aussi sa patience.

Je tiens également à remercier très chaleureusement M. Ali Sarraf Moghaddam, mon très
cher enseignant de biologie qui m’a gentiment familiarisé avec les sciences de la nature,
un grand merci toujours pour ses encouragements, ses qualités humaines rares dont la
gentillesse.
J’exprime ma sincère gratitude à M. Dr. Kiabi, mon très cher professeur d’Université en
Iran, qui m’a appris l’esprit de la recherche scientifique, celui du travail en équipe,
l’autonomie et la modestie dans le travail, tout en pensant à notre futur et en nous
ouvrant à des opportunités de continuation dans le domaine de la recherche. Je tiens à le
remercier pour ses conseils qui m’aident chaque jour.
Un grand remerciement à mes deux très chers amis et collègues, M. Hamid-Reza Rezaei
et M. Hamid-Reza Naghash, pour leur amitié, ainsi que pour les bons moments où nous
avons travaillé ensemble. J’espère que nous pourrons de nouveau travailler ensemble
dans le futur.
J’adresse mes sincères remerciements à tous ceux qui m’ont aidé pour l’échantillonnage
en Iran, surtout M. Hamid-Reza Rezaei, M. Hamid-Reza Naghash, M. Javad Ramezani,
M. Ebrahim Ghaderi, M. Afshin Karami, M. Rasul Marsouli, M. Abbas Rafat ainsi
qu’aux agents de l’Organisation pour l’Environnement et la conservation en Iran, qui par

-I-
leur dévouement m’ont apporté une aide inestimable sur le terrain. Un remerciement tout
particulier à M. RamazanAli Ghaemi et M. Bijan Farhang Darehshoori pour leurs avis
d’experts. Sans le dévouement, l’aide et le soutien de vous tous, un échantillonnage à si
grande échelle n’aurait pu être possible.
Je tiens également à remercier sincèrement M. Aykut Kence, M. Deniz Ozut, Mme Ozge
Balkiz, M. Paul Weinberg et M. Amjad Tahir Virk, pour leurs échantillons de Turquie,
Azerbaidjan, Dagestan, Turkménistan et Pakistan.
Ensuite, beaucoup de manips n’auraient pu être réalisées sans l’aide de mes collègues,
Christian, Delphine, Stéphanie, Ludovic, Carole. Mille mercis à eux.
Je tiens à remercier tous mes collègues du LECA. C’est avec joie que j’ai partagé ces
quatre années avec eux. Que tous mes collègues, Carole, Christian, Patrik, Cyrille, Alice,
Bahar, Olivier, Mihai, Julien, Sébastien, Delphine, Stéphanie, Ludovic, Margot,
Bénédicte, Pierre, Matthieu, Morana, Toni, Florence, Jean-Marie, Olivier, Anthony,
Wasim et …, ne soient pas oubliés pour leur collaboration et leur contribution à
l’ambiance bien sympathique du laboratoire.
Je tiens à remercier tout particulièrement Christian et Carole pour leurs qualités
humaines extraordinaires, leur gentillesse. Ce fût pour moi une suite d’encouragements.
Je dois grand remerciement également à Dr. Jean-Denis Vigne et Dr. Marjan Mashkour
pour leurs aides en partie d’Archeaozoology et aussi Dr. Michael Blum et Dr. Ricardo
Negrini pour leurs aides en analyse de données.
Je remercie très sincèrement Marjan Mashkour, Catherine Hänni, Sandrine Hughes,
Héléna Fernández pour l’intérêt qu’elles ont porté à mon travail et leurs précieux
conseils lors des comités de thèse.
Je remercie tous les professeurs et chercheurs du LECA, Irène, Philippe, Roberto, Oscar,
Laurence, Serge et…, pour leurs discussions scientifiques qui m’ont guidé au cours de
mon travail, et toujours dans une ambiance bien sympathique.
De même, je remercie les membres de l’équipe de foot du LECA, pour leur amitié et
pour tous les fantastiques moments passés ensemble dans une excellente ambiance, qui
m’ont donné la santé et la motivation pour la bonne continuation de ma thèse : Cyrille,
Seb, Fred, Julien, Tarafa, Ozgur, Abdé, Amandine, Margot, Michael, Jérôme, Thierry,…

Je remercie tous mes amis iraniens pour leur soutien et pour tous les fantastiques
moments passés ensemble qui sont vraiment pour moi parmi les meilleurs souvenirs de
ma thèse tout au long de mon séjour en France, particulièrement à Grenoble.

J’adresse mes remerciements très chaleureux à tous mes amis iraniens, Abbas
Akbaripasand, Alireza mirzajani, Reza Amini, Javad Ramezani, Mehrdad Khoshchin,
Ayoub Dadbaz, Hossein Najari, Ali Masood Evaz, Abbas Pahlavani, Hassan Rajabi,
Rasul Fesharakifard, Babak Nosrati, Ahmad Amini, Mohammad Hassani, Mohammad-
Reza Nahal Tahmasbi, Seyed Mojtaba Vaezi, Ali Zamanifard, … pour leur amitié et le
soutien moral permanent de proche ou de loin.

Je tiens évidement à remercier mes parents, mes sœurs pour m’avoir suivi dans
l’inconnu, pour m’avoir soutenu et pour m’aimer autant; leur bienveillance permanente
et leur amour inconditionnel sont mes joies et mes espoirs.

J’adresse mes remerciements plus particulièrement à ma chère épouse, Simin, qui a été
toujours présente à mes côtés, à tous les instants pour m’apporter son aide, son soutien et
son amour pour pouvoir franchir les plus durs moments de ma thèse. Je n’y serais pas
arrivé sans toi, cette thèse c’est aussi la tienne.

- II -
Abbreviations

ADN-mt ADN mitochondrial

AFLP Amplified Fragment Length Polymorphism
AMOVA Analysis of Molecular Variance
Bp Base pair
Ca. Circa
Cal. B.P. Calibrated Before Present
CI Confidence Interval
Cytb Cytochrome b
dNTP di-desoxy Nucleotide Tri Phosphate
D-loop Displacement-loop
ESUs Evolutionary Significant Units
FCA Factorial Correspondence Analysis
HVI Hyper Variable I
indel insertion/deletion
K2P Kimura 2-Parameters
mtDNA mitochondrial DNA
MB MrBayes
ML Maximum Likelihood
Myr, MYA Million Years , Million Years Ago
NJ Neighbour Joining
Pb paire de base
PCR Polymerase Chain Reaction
PPNB PrePottery Neolithic B
SNP Single Nucleotide Polymorphism
TBR Tree Bisection Reconnection
TMRCA Time to the Most Recent Common Ancestor
Ts Transitions
Tv Transversion
YBP Years Before Present

- III -
Table of Contents

Abbreviations ..................................................................................................................III
Table of Contents............................................................................................................IV
List of Figures .............................................................................................................. VIII
List of Tables ................................................................................................................ XIII
Chapter 1. Version abrégée en français: Histoire évolutive de l’Aegagre (Capra
aegagrus) et de la chèvre ([Link]) basée sur l’analyse du polymorphisme de l’ADN
mitochondrial et nucléaire: Implications pour la conservation et pour l’origine de la
domestication....................................................................................................................14
1. Les outils pour comprendre l’origine des animaux domestiques et pour mesurer leur
diversité.............................................................................................................................14
1.1. Caractérisation moléculaire ...................................................................................14
1.2. Approches archéobiologiques................................................................................15
2. Biodiversité des animaux domestiques.........................................................................16
3. Etudes portant sur la chèvre..........................................................................................18
4. La Domestication..........................................................................................................19
5. Génétique de la conservation........................................................................................21
Article 1. Analyse à grande échelle de la diversité génétique chez la chèvre domestique
..........................................................................................................................................22
Article 2. Arguments génétiques en faveur d’un événement de domestication à grande
échelle chez la chèvre .......................................................................................................26
Article 3. Les vaches, les moutons et les chèvres sont-elles des espèces menacées? ......31
Conclusion ........................................................................................................................32
Chapter 2. Introduction .................................................................................................35
1. Tools to understand livestock origin and diversity..................................................37
1.1. Genetic tools ..........................................................................................................37
1.1.1. Choosing molecular markers ..........................................................................38
1.1.2. Mitochondrial DNA........................................................................................38
1.1.3. Amplified fragment length polymorphism (AFLP)........................................40
1.1.4. Y-chromosome DNA......................................................................................41
1.1.5. Microsatellites.................................................................................................42
1.2. Archaeobiological approaches...............................................................................44
1.2.1. Ancient DNA ..................................................................................................44
1.2.2. Archaeological markers ..................................................................................45
[Link]. Morphological Markers ...........................................................................45
[Link].1. Genetically driven markers...............................................................45
[Link].2. Plastic Responses to domestication ..................................................46
[Link]. Non-morphological Markers ...................................................................46
[Link].1. Demographic profiling......................................................................46
[Link].2. Zoogeography and abundance ..........................................................47
[Link].3. Different types of more circumstantial evidence of human control .47
2. Livestock biodiversity.................................................................................................48
2.1. Current knowledge.................................................................................................48
2.1.1. Species diversity .............................................................................................48
2.1.2. Breed diversity................................................................................................49
2.2. Livestock’s genetic diversity .................................................................................51
2.3. Goat and its general situation ................................................................................51

- IV -
 2.4. Goat genetics diversity results, up to now .............................................................52
3. Domestication..............................................................................................................54
3.1. The domestication process in general....................................................................54
3.2. Domestication history............................................................................................55
3.3. Domestication centers............................................................................................57
3.4. Complex patterns of genetic structure of domesticates .........................................59
3.5. Goat Domestication ...............................................................................................60
4. Livestock transformations following domestication and consequences on genetic
diversity ...........................................................................................................................63
5. Conservation Genetics and implications for conservation......................................65
Chapter 3. Large-scale mitochondrial DNA analysis of the domestic goat reveals six
haplogroups with high diversity ....................................................................................66
Abstract.........................................................................................................................67
Introduction...................................................................................................................68
Results...........................................................................................................................70
Sequence polymorphism...........................................................................................70
Phylogenetic analysis and genetic structure of domestic goats ................................70
Demography of mitochondrial haplogroups.............................................................76
Discussion.....................................................................................................................78
High mtDNA diversity in domestic goat ..................................................................78
Characteristics and nomenclature of mitochondrial haplogroups ............................78
Standard criteria for defining goat mitochondrial haplogroups................................79
Genetic structure of domestic goats..........................................................................81
Demography of mitochondrial haplogroups.............................................................82
Limits of genetic data from domestic goats for reconstituting the history of
domestication............................................................................................................83
Materials and methods..................................................................................................84
Sampling and DNA extraction..................................................................................84
DNA amplification and sequencing..........................................................................84
Data analysis.............................................................................................................85
Acknowledgements.......................................................................................................86
References.....................................................................................................................87
Chapter 4. Goat domestication: a single large-scale event without bottleneck.........91
METHODS SUMMARY..........................................................................................100
Mitochondrial DNA analyses .................................................................................100
Estimation of population growth rate .....................................................................100
Estimation of the number of goat mtDNA haplotypes captured during the
domestication process.............................................................................................100
Nuclear DNA analysis ............................................................................................100
Acknowledgements.....................................................................................................104
METHODS................................................................................................................105
Mitochondrial DNA analyses .................................................................................105
Sampling .............................................................................................................105
DNA extraction...................................................................................................105
DNA amplification .............................................................................................105
DNA sequencing.................................................................................................106
Data analysis.......................................................................................................106
Estimation of population growth rate .................................................................107
Estimation of the number of goat mtDNA haplotypes that were captured during
the domestication process ...........................................................................107

-V-
 Phylogenetic approach....................................................................................107
Rarefaction analysis of the number of goat mtDNA haplotypes found
according to the number of samples analyzed................................................108
Estimation of the Time to the Most Recent Common Ancestor (TMRCA) for the
different goat haplogroups..........................................................................108
Computation of the pairwise coalescence times .................................................108
Frequency of the A haplogroup at the time of the domestication.......................108
Nuclear DNA analysis ............................................................................................109
Sampling .............................................................................................................109
DNA extraction...................................................................................................109
AFLP procedure..................................................................................................109
Data analysis.......................................................................................................109
SUPPLEMENTARY INFORMATION..................................................................112
Supplementary results..........................................................................................112
Partitioning of the mtDNA genetic variance within and among localities .........112
Estimation of the number of goat mtDNA haplotypes that have been captured
during the domestication process................................................................112
Phylogenetic approach........................................................................................112
Rarefaction analysis of the number of goat mtDNA haplotypes found according
to the number of samples analyzed.............................................................113
Estimation of the TMRCA for the different goat haplogroups...........................113
Computation of the pairwise coalescence times. ................................................113
Frequency of the A haplogroup at the time of the domestication.......................113
Nuclear DNA analysis ........................................................................................113
Supplementary Discussion ...................................................................................113
Introgression from the domestics to the wilds in southeastern Iran ...................113
Number of mtDNA haplotypes captured during the domestication process ......114
Supplementary Tables and Figures ....................................................................116
Chapter 5. Are cattle, sheep, and goats endangered species?...................................151
Abstract.......................................................................................................................152
Introduction.................................................................................................................152
Wild ancestors and the domestication process ...........................................................154
Cattle.......................................................................................................................154
Sheep.......................................................................................................................155
Goats .......................................................................................................................155
Dispersal from the domestication centres...................................................................156
The threats on highly productive breeds.....................................................................158
Fragmentation into discrete breeds .........................................................................158
Effects of artificial insemination and other reproductive technologies ..................159
The threats on local breeds with low population sizes ...............................................162
Socio-economic context..........................................................................................162
Management of small size populations...................................................................162
Threats to adaptation...............................................................................................163
Geographic confinement.........................................................................................164
Conclusion ..................................................................................................................164
References...................................................................................................................167
Discussion and Conclusion...........................................................................................173
Perspectives ...................................................................................................................175
Bibliography..................................................................................................................176
Annex .............................................................................................................................193

- VI -
Review of archaeozoological data for the earliest goat domestication.......................194
Eastern Anatolian area............................................................................................194
Iranian Plateau ........................................................................................................198
References...............................................................................................................201

- VII -
List of Figures

Figure 1.1. Arbres phylogénétiques non racinés réalisé avec la méthode Neighbor-
joining et démontrant le polymorphisme de l’ADNmt pour 744 vaches, 640 moutons et
1813 chèvres (Taberlet et al. 2007). .................................................................................17
Figure 1.2. Distribution géographique des taxons sauvages du genre Capra. (d'après
Pidancier et al. 2006, modifié). ........................................................................................18
Figure 1.3. Principaux centres de domestication en fonction de données génétiques et
archéologiques d’après la FAO (2007) (1) dinde - (2) cobaye, lama, alpaga - (3) cochon,
lapin - (4) vache, âne - (5) vache, cochon, chèvre, mouton, chameau - (6) vache, chèvre,
poulet, buffle - (7) cheval - (8) yack - (9) cochon, buffle, poulet – (10) poulet, cochon,
vache - (11) dromadaire, (12) renne. ................................................................................20
Figure 1.4. Capra aegagrus.............................................................................................21
Figure 1.5. A. Les six haplogroupes mitochondriaux de chèvres domestiques détectés à
partir de l’analyse de 1540 haplotypes (A, B, C, D, F, G). L’arbre représenté a été réalisé
par la méthode de Neighbor-Joining. Les chiffres donnent les valeurs de bootstraps. Les
étoiles représentes la position de 22 individus choisis comme références représentant la
diversité totale et dont l’arbre neighbor-joining est donné dans l’encadré B. ..................23
Figure 1.6. Distribution géographique des haplogroupes d’ADNmt chez la chèvre
domestique........................................................................................................................24
Figure 1.7. Distribution des substitutions entre paires d’haplotypes pour les
haplogroupes d’ADNmt....................................................................................................25
Figure 1.8. Relations phylogénétiques des 251 aegagres et des 22 haplotypes de
référence représentatifs de la diversité des chèvres. Les haplotypes des six haplogroupes
définis chez les domestiques sont représentés par: vert = A, bleu foncé = B, jaune = C,
rose = D, bleu clair = F et orange = G. Les haplotypes rouges correspondent aux
sauvages proches des domestiques, ceux représentés en blanc correspondent aux
sauvages n’appartenant pas à un haplogroupe domestiqué. .............................................27
Figure 1.9. Région étudiée et distribution géographique des haplogroupes d’ADNmt
pour l’aegagres. a) Distribution naturelle du aegagre d’après Uerpmann (Uerpmann
1987). Les sites archéologiques qui démontrent la domestication pré-Néolithique locale
de chèvre sont représentés en rouge. Les sites qui suggèrent la domestication locale de la

- VIII -
chèvre, ou le transfert de chèvres domestiquées au début de la période néolithique dite de
« pré-poterie », sont représentés en orange. Les sites qui fournissent l'évidence d’un
transfert de chèvres hors de la région géographique originelle de l’aegagre vers le milieu
du 10 ème millénaire Cal. B. P, sont représentés en jaune. b) Distribution géographique
des haplogroupes de mtDNA pour l’aegagre. La taille des cercles est proportionnelle au
nombre d'individus analysés. Les différents haplogroupes d’aegagre sont en codes
couleurs identiques à ceux utilisés pour la Figure 1.4. Les différentes localités identifiées
par des nombres, correspondent à celles décrites dans le tableau n°1 annexé à l’article
n°2.....................................................................................................................................29
Figure 1.10. Capra aegagrus à Malayer, Zone Protégée en Iran. ...................................34
Figure 2.1. Schema of the Mammalian mitochondrial genome.......................................40
Figure 2.2. Global distribution of five major domestic species: cattle, sheep, chickens,
goats, and pigs. .................................................................................................................49
Figure 2.3. Distribution of the world’s mammalian breeds by species ...........................50
Figure 2.4. Archaeological map of agricultural homelands and spread of
Neolithic/Formative, with approximate radiocarbon dates (Diamond & Bellwood 2003).
..........................................................................................................................................56
Figure 2.5. Major centres of livestock domestication, based on archaeological and
molecular genetic information..........................................................................................58
Figure 2.6. Map of goats introduction routes from their initial domestication areas into
Europe along ‘‘Mediterranean’’ and ‘‘Danubian’’ route. (From Guilaine 2003;
Fernández et al. 2006). .....................................................................................................62
Figure 2.7. The habitat of Capra aegagrus in Dena Protected area in Iran .....................65
Figure 3.1. Neighbor-joining trees of domestic goat based on 1540 mtDNA haplotypes
(A) and on the 22 reference mtDNA haplotypes (B). Distances were calculated using the
Kimura 2-Parameter model with gamma correction (alpha = 0.28). On the (A) tree, the
numbers on the branches represent bootstrap values out of 1000 replications, and the
stars point out the position of reference individuals for each haplogroup used to construct
the (B) tree (see Table 3.5). ..............................................................................................71
Figure 3.2. Geographic distribution of domestic goat mtDNA haplogroups. The size of
each circle is proportional to the sample size and each specific haplotype is represented
by a different colour..........................................................................................................73

- IX -
Figure 3.3. Mismatch distributions for mtDNA haplogroups of domestic goats. For the
overall dataset, the distribution of pairwise differences were realized separately for
comparisons between and within haplogroups. ................................................................77
Figure 4.1. Phylogenetic relationship of the 251 haplotypes from the 487 bezoars
studied. This tree was obtained with the neighbour joining method (see Methods). In
order to identify shared mtDNA haplogroups, 22 haplotypes chosen to represent the
overall diversity of modern goats13 have also been included in the analysis (in red). The
scale represents the genetic distance. The different colors correspond to the haplotypes
from the different mtDNA haplogroups found in goat (A: green, B: dark blue, C: yellow,
D: purple, F: light blue, G: orange). The other bezoar haplotypes are represented in
white. ................................................................................................................................94
Figure 4.2. Study area and geographic distribution of the mtDNA haplogroups in the
bezoar. a, Natural distribution of the bezoar according to Uerpmann28. This distribution
may not have changed since the beginning of goat management/domestication, and stops
at the Eastern limit of the map. The archaeological sites that give evidence of local pre-
Neolithic goat domestication are represented in red. (Figure 4.2, continued) The sites that
suggest either local goat domestication or early pre-pottery Neolithic transfer of
domesticated goat are represented in orange. Finally, the sites that provide evidence of
transfer of goats out of the original geographic range of the bezoar before the middle of
the 10th millennium cal. B.P. are represented in yellow (Supplementary Table 4.3). b,
Geographic distribution of the mtDNA haplogroups in the bezoar. The size of the circles
is proportional to the number of individuals analyzed. The different bezoar haplogroups
are color-coded as in Figure 4.1. Different localities are identified by numbers, as in
Supplementary Table 4.1. .................................................................................................96
Figure 4.3. Phylogenetic tree (neighbour joining) of the C haplogroup in both goats (in
red) and bezoar (light green from Eastern Turkey, dark green from other locations). This
tree was obtained with the neighbour joining method (see Methods). The close
relationships between bezoars from Eastern Turkey and goats demonstrates that the
domestication for the C haplogroup occurred in this area. The domestic goat C
haplotypes are grouped into at least three clusters, suggesting at least three ancestral
haplotypes. The numbers represent the populations as in Figure 4.2b and Supplementary
Table 4.1. ..........................................................................................................................98
Figure 4.4. Capra aegagrus in Golestan National Park in Iran.....................................103

-X-
Supplementary Figure 4.1. Number of ancestral haplotypes at the time of domestication
as a function of the size of the sample. The dots correspond to the bootstrap replicates
and the curves have been obtained using a polynomial regression. ...............................143
Supplementary Figure 4.2. Pairwise coalescence times of goat (Capra hircus) mtDNA
haplotypes. Genetic distances are computed as the number of differences between pairs
of sequences and are then rescaled in time by using 250,000 years for the divergence
time between A and C haplogroups. The shaded part of the histogram corresponds to the
pairs of sequences that coalesced more recently than the domestication. ......................144
Supplementary Figure 4.3. Probability of observing more than the present number of
individuals from the A haplogroup as a function of the frequency of the individuals from
the A haplogroup at the time of the domestication.........................................................145
Supplementary Figure 4.4. Levels of genetic polymorphism of nuclear DNA inferred
from AFLP analysis for the bezoar (Capra aegagrus) and for eight goat (Capra hircus)
breeds, five from Iran, three from Italy. .........................................................................146
Supplementary Figure 4.5. Placement of the bezoars of the A haplogroup from the Lar
Mountains (Southeast Iran, locality 33 in Figure 2b) within the phylogeny of the A
haplogroup of goats. The presence of bezoar haplotypes (in green) in many different
clades of the phylogeny indicates a likely introgression from the domestics to the wilds.
........................................................................................................................................147
Supplementary Figure 4.6. The habitat of Capra aegagrus in Dahaj protected area in
Iran..................................................................................................................................150
Figure 5.1. Unrooted neighbor-joining trees showing the mtDNA polymorphism of
cattle, sheep, and goats. The phylogenetic analyses were conducted using MEGA version
3.1, Kumar et al. 2004, with control region sequences. A total of 744 sequences from
Loftus et al. 1994, Bradley et al.1996, and Troy et al. 2001 were used for cattle. A total
of 640 sequences from Wood & Phua 1996, Hiendleder et al. 1998, Guo et al. 2005,
Pedrosa et al. 2005, Meadows et al. 2006, and Tapio et al. 2006 were used for sheep. A
total of 1813 sequences from Luikart et al. 2001, Sultana et al. 2003, Joshi et al. 2004,
Azor et al. 2005, Chen et al. 2005, Odahara et al. 2005, Pereira et al. 2005, Li et al.
2006, Sardina et al. 2006, and Liu et al. 2007 were used for goats. The letters A, B, C,
etc. in the trees for sheep and goats represent the different mtDNA haplogroups
described in the literature................................................................................................157

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Figure 5.2. The two main initial advancements of the Neolithic culture into Europe
(from Fernàndez et al. 2006). The dates on the map are calibrated radiocarbon date-
derived BP, and correspond to the arrival of agriculture in the corresponding region...158

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List of Tables

Table 2.1. Status of information in the Global Databank for Animal Genetic Resources
(FAO 2007).......................................................................................................................50
Table 2.2. Summary of genetic and archaeological information for different domestic
species (FAO 2007) ..........................................................................................................59
Table 3.1. Genetic diversity of goat mtDNA haplogroups ..............................................72
Table 3.2. Geographic origin and characteristics of the studied domestic goat...............74
Table 3.3. Partition of the genetic variance among haplogroups, breeds and continental
regions revealed by hierarchical AMOVAs .....................................................................76
Table 3.4. Estimation of demographic parameters from genetic data .............................78
Table 3.5. The 22 reference individuals of the 6 domestic goat haplogroups .................80
Table 4.1. Estimation of population growth rates (most probable estimates) for domestic
goat and for two categories of bezoar (wilds close-to-domestics; wilds non close-to-
domestics) using Lamarc v2.225. ......................................................................................95
Supplementary Table 4.1. Geographic origin and characteristics of the wild goat
samples for mt-DNA sequence study. ............................................................................116
Supplementary Table 4.2. Geographic origin and characteristics of the domestic and
wild goat samples used for AFLP study. ........................................................................132
Supplementary Table 4.3. Additional information about the archeological sites
indicated in Fig. 2a. ........................................................................................................141
Supplementary Table 4.4. Partition of the genetic variance among geographic regions
and populations by Analysis of molecular variance for bezoars (Capra aegagrus). .....142
Supplementary Table 4.5. TMRCA for different mtDNA haplogroups of goats (Capra
hircus). ............................................................................................................................142
Table 5.1. Population sizes, current number of breeds, number of extinct breeds for
cattle, sheep, and goats in different regions (source: FAOSTAT from Scherf (2000);
statistics concerning 170 countries)................................................................................153
Table 5.2. Examples of effective population sizes in some cattle breeds......................160

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Chapter 1. Version abrégée en français
Chapter 1 Version abrégée en français

Chapter 1. Version abrégée en français: Histoire évolutive de l’Aegagre

(Capra aegagrus) et de la chèvre ([Link]) basée sur l’analyse du
polymorphisme de l’ADN mitochondrial et nucléaire : Implications pour la
conservation et pour l’origine de la domestication

1. Les outils pour comprendre l’origine des animaux domestiques et pour mesurer
leur diversité

1.1. Caractérisation moléculaire

La diversité génétique des espèces est la conséquence des évènements génétiques et

démographiques qui ont eu lieu durant son évolution. La structure actuelle de cette
diversité garde la signature de ces évènements, ce qui nous permet de reconstituer
l’histoire évolutive. Parmi les facteurs environnementaux qui affectent l’évolution des
espèces, l’homme tient une place particulière. Il exerce des contraintes sélectives directes
ou indirectes sur un bon nombre d’espèces. Un type de relation particulier s’est établi entre
l’Homme et certains organismes dans le cadre du processus de domestication. Si l’on ne
prend en compte que les espèces animales, plus de 40 d’entre elles sont aujourd’hui
domestiquées (FAO 2006).
La diversité génétique de ces espèces résulte des processus génétiques et
démographiques liés à l’histoire de leur domestication. Elle dépend par exemple de leur
dispersion géographique qui s’est faite à travers le monde en suivant les migrations
humaines, des flux géniques qui ont découlés des échanges commerciaux. Dans ce
contexte de flux géniques constants mais assez faibles, plusieurs milliers d’années de
sélection ont conduit à l’adaptation de races locales à leur environnement. Ces races
locales, ainsi que les espèces sauvages proches des domestiques représentent cependant
une ressource génétique inestimable. Depuis quatre à cinq décennies, cette vaste diversité
intra-spécifique se réduit fortement par le remplacement progressif de ces races locales par
un petit nombre de races industrielles, sélectionnées. Ainsi l’analyse de la diversité
génétique des espèces domestiques et de leurs proches ancêtres sauvages permet de
reconstituer l’histoire de la domestication et a également des applications dans la gestion
des ressources génétiques.

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Chapter 1 Version abrégée en français

Le polymorphisme de l’ADN (marqueurs nucléaire et mitochondriaux) est utilisé

pour mesurer la diversité génétique des animaux domestiques. La plupart des études ne
concernent pas les gènes responsables de caractères dont la variation est liée au processus
de domestication. Elles se focalisent plutôt sur l’analyse du polymorphisme neutre afin de
permettre la reconstitution de l’histoire évolutive des espèces domestiques et de leurs
ancêtres sauvages (Zeder et al. 2006a).
Le marqueur moléculaire idéal pour étudier l’origine de la domestication doit être
suffisamment conservé pour permettre l’identification des taxons sauvages à l’origine des
espèces domestiques. Mais il doit également être suffisamment variable et structuré
géographiquement pour permettre de localiser les lieux de domestication. Son évolution
doit aussi se faire à un taux constant. Il est difficile de trouver un marqueur parfait,
cependant plusieurs zones de l’ADN mitochondrial approchent la plupart de ces
conditions. C’est pour cela que les marqueurs mitochondriaux sont de loin les plus utilisés
pour les études moléculaires sur les animaux domestiques (Bruford et al. 2003).

1.2. Approches archéobiologiques

La combinaison des approches archéologiques et génétiques a conduit depuis une

vingtaine d’années à une véritable explosion des connaissances sur l’origine de la
domestication. Les études d’ADN ancien permettent de génotyper les ossements retrouvés
sur les sites archéologiques. De telles données nous informent sur l’origine et les routes
migratoires des espèces domestiques (Fernández et al. 2005). L’étude des variations de la
diversité génétique au cours du temps chez les domestiques et les sauvages sont utiles pour
tenter de distinguer les phénomènes de domestication locale des introgressions à partir des
animaux domestiques (Luikart et al. 2006).
Les études archéologiques apportent des données complémentaires qui concernent
directement les animaux (morphologie) mais aussi leur environnement (contexte
écologique) et l’Homme qui les a domestiqués (outils en relation avec le processus de
domestication). Les caractères morphologiques mesurés peuvent être modifiés en raison
d’une réponse adaptative aux forces sélectives résultant de la domestication (marqueurs
Animal-orientés). Ils reflètent donc l’impact évolutif de la domestication sur les
populations. D’autres caractères peuvent être modifiés dans le cadre d’une réponse
plastique du phénotype. Les variations morphologiques varient alors en nature et en
intensité en fonction de facteurs locaux et peuvent changer rapidement au cours du temps.

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Chapter 1 Version abrégée en français

D’autres marqueurs ne sont pas liés aux animaux et démontrent l’existence d’un
contrôle et d’une gestion des troupeaux par l’Homme (marqueurs Humain-orientés). Ces
types d’indices sont particulièrement intéressants quand ils précèdent les réponses
morphologiques adaptatives des animaux à la domestication. Ils peuvent consister en des
outils, des restes de corrals (Zeder et al. 2006a).
La caractérisation démographique apporte aussi des informations importantes. Elle
est basée sur l’hypothèse que l’âge et le sexe des animaux tués par des chasseurs diffère de
celui des animaux capturés par des gardiens de troupeaux, car les deux modes de capture
ne répondent pas aux mêmes contraintes. Des données ostéométriques à partir desquelles
on caractérise l’âge et le sexe des restes d’animaux sur les sites archéologiques permettent
de distinguer la gestion de troupeaux de différentes pratiques de chasse (sélective et non
sélective).
Enfin, des données d’abondance et de biogéographie sont également informatives.
L’apparition d’espèces potentiellement domestiques en dehors de leur aire de répartition
naturelle est généralement interprétée comme résultant de mouvements contrôlés par
l’Homme. Ces mouvements auraient concerné des troupeaux domestiques, mais aussi des
animaux sauvages en cours de domestication (Zeder 2006).

2. Biodiversité des animaux domestiques

Depuis plus de 10 000 ans, les mutations, l’adaptation locale, la dérive génétique et la
sélection des races ont modelé la diversité génétique des populations domestiques. Ces
mécanismes ont concerné une quarantaine d’espèces sur les 50 000 que nous connaissons
chez les oiseaux et mammifères. Au total, 7 616 races ont été identifiées, la majorité
d’entre elles étant originaires d’Europe et d’Asie (FAO 2007).
Chez la vache, la chèvre et le mouton, on trouve un haut niveau de polymorphisme
de l’ADN mitochondrial. Pour chaque espèce, l’existence de plusieurs haplogroupes est le
résultat de multiples origines maternelles (Figure 1.1). Ces origines multiples peuvent
découler de plusieurs évènements de domestication en différents lieux et/ou à différentes
périodes, ou bien de la capture de plusieurs haplotypes au cours d’un unique événement de
domestication. Le polymorphisme nucléaire est également élevé (e.g. Maudet et al. 2002),
comparable à celui trouvé chez les espèces sauvages (Taberlet et al. 2007). Il apparaît
également que la diversité des espèces animales domestiques est en premier lieu répartie
selon un axe Est-Ouest (MacHugh & Bradley 2001).

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Chapter 1 Version abrégée en français

Figure 1.1. Arbres phylogénétiques non racinés réalisés avec la méthode Neighbor-joining
et démontrant le polymorphisme de l’ADNmt pour 744 vaches, 640 moutons et 1813
chèvres (Taberlet et al. 2007).

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Chapter 1 Version abrégée en français

3. Etudes portant sur la chèvre

Le genre Capra est composé de la chèvre et des espèces sauvages apparentées :

l’Aegagre, le Markhor, les Bouquetins et les Turs. Si l’on excepte l’espèce domestique, le
genre est uniquement présent dans l’ancien monde. Les données fossiles suggère une
origine en Asie Centrale suivie d’une radiation au Plio-pleistocene. Peu de données
archéologiques sont disponibles pour ces espèces, leurs habitats montagnards étant peu
propices à la conservation des fossiles. Il en résulte une histoire évolutive mal connue,
sans doute également à cause de la rapidité de la radiation du genre, qui rend difficile
l’inférence des relations phylogénétiques entre espèces. Le nombre et le statut des taxons
composant le genre Capra fait encore débat, et l’on définit de 6 à 9 espèces (Figure 1.2,
Pidancier et al. 2006).

Figure 1.2. Distribution géographique des taxons sauvages du genre Capra. (d'après
Pidancier et al. 2006, modifié).

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Chapter 1 Version abrégée en français

Les études sur la diversité génétique de la chèvre domestique (Capra hircus) ont
permis de définir jusqu’à présent 6 haplogroupes mitochondriaux. (Luikart et al. 2001;
Sultana et al. 2003; Joshi et al. 2004). La plupart de cette diversité apparaît au sein des
groupes, et seulement 10% est due aux différences entre continents. Luikart et al. (2001)
ont estimé le temps de divergence entre haplogroupes à plus de 200 000 ans, bien avant le
moment de la domestication. Cela suggère que la diversité observée aujourd’hui ne
provient pas uniquement d’une population unique qui aurait existé il y a 10 000 ans. La
structuration géographique de la diversité génétique de la chèvre est plus nette avec des
marqueurs microsatellites qui montrent qu’une grande proportion de la diversité génétique
qui existe entre races s’explique par l’origine géographique (Cañon et al. 2006).
La diversité génétique passée a également pu être mesurée à partir d’étude d’ADN
ancien, qui montrent l’origine et les routes de migration des différents haplogroupes du
Moyen-Orient vers l’Europe. Jusqu’alors deux des haplogroupes définis actuellement (A
et C) ont été retrouvés dans des sites archéologiques (Fernández et al. 2006).

4. La Domestication

La domestication est un phénomène complexe et graduel qui trouve son origine dans
la propension des chasseurs-cueilleurs à l’apprivoisement et à la gestion des animaux
sauvages. A la fin du Pléistocène, le climat est devenu plus chaud avec des saisons plus
marquées. Cela a accru la nécessité de nourriture stockable et la mise en place de cultures
et d’élevages. Ces phénomènes ont commencé au début du Néolithique il y a 12 000 à 14
000 ans et ont conduit à la révolution agricole (Diamond 2002). En ce qui concerne les
animaux d’élevage, au moins une douzaine de centres de domestication ont été mis en
évidence à travers le monde (FAO 2007).

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Chapter 1 Version abrégée en français

Figure 1.3. Principaux centres de domestication en fonction de données génétiques et

archéologiques d’après la FAO (2007) (1) dinde - (2) cobaye, lama, alpaga - (3) cochon,
lapin - (4) vache, âne - (5) vache, cochon, chèvre, mouton, chameau - (6) vache, chèvre,
poulet, buffle - (7) cheval - (8) yack - (9) cochon, buffle, poulet – (10) poulet, cochon,
vache - (11) dromadaire, (12) renne.

Les analyses génétiques ont montré une grande diversité des processus de
domestication, en terme nature et nombre de progéniteurs ayant contribué au pool
génétique de l’espèce domestiquée (Bruford et al. 2003).
La chèvre a été parmi les premiers animaux d’élevage domestiqués, il y a plus de
10 000 ans, contribuant à la révolution Néolithique (Zeder & Hesse 2000). Les
connaissances acquises sur la domestication de la chèvre nous permettent de mieux
comprendre l’origine et la propagation de l’agriculture. Les données archéologiques et
morphologiques suggèrent que la chèvre a été domestiquée à partir de l’aegagre (Capra
aegagrus) dans le Croissant Fertile (e.g. Peters et al. 1999; Peters et al. 2005; Zeder 2005)
Cette origine a été confirmée par des études génétiques basées sur l’analyse d’ADN
mitochondrial et nucléaire (Luikart et al. 2006; Takada et al. 1997). Les données
archéologiques situent la domestication il y a environ 10 500 ans dans les vallées de
l’Euphrate et du Tigre, dans le Sud-Est de l’Anatolie (Peters et al. 1999; Peters et al. 2005)
et entre 9 900 et 9 500 ans dans les Monts Zagros à l’Ouest de l’Iran (Zeder & Hesse
2000; Zeder et al. 2005; Zeder et al. 2006b). La transition de la chasse à la gestion de
troupeau est marquée par la capture très majoritaire de jeunes mâles sub-adultes. Les
chèvres de cette période ressemblaient sans doute beaucoup aux aegagres sauvages, du
point de vue morphologique et génétique. Quelques 500 ans plus tard, les hommes et leur
cheptel quittèrent ces montagnes vers les plaines voisines qui constituaient des
environnements défavorables à la vie des aegagres. La migration vers ces plaines mit un

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Chapter 1 Version abrégée en français

terme à la possibilité d’hybridation entre les animaux domestiques et sauvages. Il est

possible que, couplé à cette interruption du flux génique, les conditions plus arides et les
pâtures plus pauvres rencontrées dans ces nouveaux milieux aient contribué à la réduction
de taille de l’espèce domestique (Zeder 2006). De nombreux changements sont également
intervenus par la suite sous l’effet de la sélection par l’homme. Il est certain qu’une taille
plus petite rend aussi les animaux plus facilement contrôlables, et qu’elle peut être liée à
une acquisition plus précoce de la maturité sexuelle (Hall 2004).
Après ces événements initiaux, les données archéologiques nous montrent que la
culture Néolithique diffusa vers l’Europe le long de deux routes principales, la route
méditerranéenne et la route Danubienne, assurant ainsi la dispersion des chèvres
(Fernández et al. 2006).

Figure 1.4. Capra aegagrus (Photo par Saeid Naderi).

5. Génétique de la conservation

La génétique moléculaire peut être utilisée pour la gestion scientifique et la

conservation des animaux sauvages et domestiques. Il est important de mesurer la diversité
génétique des sauvages et des domestiques, de connaître les relations de parenté entre ces
espèces, leur phylogéographie, pour mettre en place des plans de conservation. La
préservation des espèces sauvages ainsi que des races locales rustiques est essentielle pour
le maintien des ressources génétiques. Une grande diversité d’allèles issue de ces stocks
pourrait être nécessaire pour renforcer la diversité génétique des races industrielles
modernes dans le cadre d’une gestion durable des élevages.

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Chapter 1 Version abrégée en français

Article 1. Analyse à grande échelle de la diversité génétique chez la

chèvre domestique

Ce chapitre est basé sur l’article “Large-scale mitochondrial DNA analysis of the
domestic goat reveals six haplogroups with high diversity” de S. Naderi, H.-R. Rezaei, P.
Taberlet, S. Zundel, S.-A. Rafat, H.-R. Naghash, M.A.A. El-Barody, O. Ertugrul6, F.
Pompanon et le consortium Econogene, publié dans PLoS ONE (PLoS ONE 2(10):
e1012. doi:10.1371/[Link].0001012).

Depuis les débuts de la domestication, le transport par l’homme des animaux

domestiques, pour des raisons économiques et commerciales, a gouverné les processus
démographiques et génétiques qui expliquent la répartition actuelle de ces animaux et la
structure génétique de leurs populations. C’est pourquoi une bonne connaissance de la
diversité génétique des animaux domestiques est un pré-requis essentiel pour la
compréhension de l’histoire de la domestication. C’est en particulier le cas pour la chèvre
qui a été l’un des premiers ongulés domestiqués en marge du Croissant Fertile il y a
environ 10 000 ans (e.g. Peters et al. 1999; Zeder & Hesse 2000; Peters et al. 2005; Zeder
2005; Luikart et al. 2006).
Dans ce cadre, cette étude a pour objectif de fournir une méthode standardisée pour
décrire la diversité actuelle des espèces domestiques, et de décrire précisément la diversité
génétique de la chèvre domestique à l’échelle mondiale. La diversité des chèvres a été
caractérisée à partir de 2430 individus provenant du monde entier. Elle inclut notamment
946 nouveaux individus provenant de régions très peu étudiées jusqu’à présent,
notamment la zone du Croissant Fertile. L’étude a porté sur le segment hyper variable HVI
de la région de contrôle de l’ADN mitochondrial. On dénote une extrême diversité de cette
région puisque les 2430 individus correspondent à 1540 haplotypes. Cette analyse ayant
été faite à l’échelle mondiale, elle permet d’établir clairement la nomenclature des
haplogroupes maternels. Selon nos résultats, seulement 5 des 6 groupes décrits jusqu’alors
sont suffisamment divergents pour pouvoir être décrits comme des haplogroupes
différents. De plus, un nouvel haplogroupe mitochondrial a été décrit, et correspond à des
individus localisés autour du Croissant Fertile (Figure 1.5 A).

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Chapter 1 Version abrégée en français

Figure 1.5. A. Les six haplogroupes mitochondriaux de chèvres domestiques détectés à

partir de l’analyse de 1540 haplotypes (A, B, C, D, F, G). L’arbre représenté a été réalisé
par la méthode de Neighbor-Joining. Les chiffres donnent les valeurs de bootstraps. Les
étoiles représentent la position de 22 individus choisis comme références représentant la
diversité totale et dont l’arbre neighbor-joining est donné dans l’encadré B.

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Chapter 1 Version abrégée en français

Une forte diversité génétique est retrouvée au sein de chacun de ces groupes. La
plupart de la diversité est répartie entre haplogroupes à l’intérieur des régions
géographiques. Cette faible structure phylogéographique résulte probablement de
l’ubiquité de l’haplogroupe A qui est fortement dominant, et représente plus de 90% des
individus (Figure 1.6). La large répartition des autres haplogroupes (à une exception près),
serait liée aux migrations humaines. L’ADN mitochondrial caractérisé ne permet pas de
distinguer la fragmentation récente des populations locales de chèvres en races isolées.

Figure 1.6. Distribution géographique des haplogroupes d’ADNmt chez la chèvre

domestique.

L’estimation des paramètres démographiques, réalisée à partir d’analyses de

mésappariements ("mismatch analysis"), montre que tous les haplogroupes ont subit une
expansion démographique récente dont la date correspond approximativement à la période
de domestication. Cependant, même avec un jeu de données aussi grand que celui utilisé

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Chapter 1 Version abrégée en français

ici, il est très difficile de donner des dates relatives exactes selon les groupes, les
intervalles de confiance étant très importants.
Au cours de cette étude, nous proposons également des critères standards pour la
définition des haplogroupes mitochondriaux. Ils sont basés en partie sur l’utilisation des
analyses de mésappariements qui permettent de définir un nombre de mutations seuil au
delà duquel les individus appartiennent à des groupes différents (Figure 1.7).

Figure 1.7. Distribution des substitutions entre paires d’haplotypes pour les haplogroupes
d’ADNmt.

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Chapter 1 Version abrégée en français

La réalisation d’un arbre phylogénétique est également nécessaire pour placer de

nouveaux individus relativement aux haplotypes déjà définis. Pour faciliter cette tâche,
nous fournissons 22 séquences de référence qui permettent une première analyse rapide de
nouveaux jeux de données (Figure 1.5 B). Cette méthodologie peut également s’appliquer
pour standardiser et clarifier la nomenclature des haplogroupes mitochondriaux chez
d’autres espèces domestiques.

Article 2. Arguments génétiques en faveur d’un événement de

domestication à grande échelle chez la chèvre

Ce chapitre est basé sur l’article “Goat domestication: a single large-scale event
without bottleneck” de S. Naderi, H.-R. Rezaei, F. Pompanon, M. G. B. Blum, R. Negrini,
H.-R. Naghash, Ö. Balkız, M. Mashkour, O. Gaggiotti, P. Ajmone-Marsan, A. Kence, J.-
D. Vigne, P. Taberlet, soumis.

Les premières traces archéologiques de la domestication de la chèvre permettent de

dater celle-ci il y a environ 10 500 ans dans les Vallées du Tigre et de l’Euphrate, dans le
Sud-Est de l’Anatolie (Peters et al. 1999; Peters et al. 2005), et il y a moins de 10 000 ans
dans le Zagros (Zeder & Hesse 2000; Zeder et al. 2005). Bien que moins probable,
l’hypothèse d’une domestication plus récente (Horwitz et al. 2000) encore dans la basse
vallée de l’Indus n’a pas été contestée (Meadow 1996). La chèvre a été domestiquée à
partir de l’aegagre (Capra aegagrus), et la mise en évidence de trois haplogroupes
mitochondriaux chez la chèvre domestique par Luikart et al. 2001, a été interprétée
comme l’existence de plusieurs évènements de domestication indépendants. En faisant
l’hypothèse d’un seul haplogroupe domestiqué par haplogroupe et en supposant un temps
de coalescence de 10 000 ans pour l’haplogroupe majoritaire (groupe A), ces auteurs ont
daté les autres évènements de domestication il y a environ 6 000 ans et 2 000 ans pour les
haplogroupes C et B respectivement. Ce scénario est complètement remis en question
depuis la découverte de la présence de chèvres de l’haplogroupe C dans le Sud de la
France il y a 7 500 ans, très loin des centres de domestication plausibles (Fernández et al.
2006).

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Dans ce contexte, notre objectif est de mieux comprendre le processus de

domestication par une analyse extensive de la diversité génétique des chèvres domestiques
et des représentants actuels de son ancêtre sauvage. Nous avons donc analysé la région de
contrôle de l’ADN mitochondrial chez 487 aegagres échantillonnés dans 43 localités
recouvrant la majeure partie de l’aire de répartition de l’espèce. Les 251 haplotypes
obtenus ont été analysés conjointement aux 1540 haplotypes domestiques connus à ce jour
(voir chapitre 4; Figure 1.8).

Figure 1.8. Relations phylogénétiques des 251 aegagres et des 22 haplotypes de référence
représentatifs de la diversité des chèvres. Les haplotypes des six haplogroupes définis chez
les domestiques sont représentés par: vert = A, bleu foncé = B, jaune = C, rose = D, bleu
clair = F et orange = G. Les haplotypes rouges correspondent aux sauvages proches des
domestiques, ceux représentés en blanc correspondent aux sauvages n’appartenant pas à
un haplogroupe domestiqué.

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Chapter 1 Version abrégée en français

Une analyse de la diversité nucléaire a également été menée en comparant à l’aide de

marqueurs AFLP le polymorphisme des aegagres à ceux de races domestiques iraniennes
et européennes (italiennes).
L’estimation de paramètres caractérisant l’histoire démographique des populations à
partir des données génétiques montre une signature d’expansion plus forte chez les
aegagres dont le génotype est proche des chèvres domestiques. Cela signifie qu’une partie
des sauvages a subit une expansion démographique avant la domestication effective, qui
pourrait être liée à une phase de gestion durable de troupeaux sauvages par l’homme. Cette
phase de pré-domestication corrobore des données archéologiques qui suggèrent le
contrôle et la protection des populations de chèvres sauvages. Elle aurait duré plusieurs
siècles. Dans le Zagros, elle aurait notamment été caractérisée par le prélèvement de
jeunes mâles et de vieilles femelles dans les troupeaux, ce qui n’était pas le cas pour les
aegagres chassés. Plus tard, les animaux issus de ces populations sauvages gérées,
éventuellement transférés loin de leur aire de distribution naturelle, auraient été à l’origine
des chèvres domestiques. La localisation actuelle des aegagres génétiquement proches des
chèvres domestiques comprend une zone qui inclut l’Est de l’Anatolie, le Zagros, le
Plateau Central Iranien et le Nord-Est de l’Iran. La phase de pré-domestication n’a donc
pas été un phénomène local, mais une pratique bien plus vaste que ne le laissait penser les
seuls arguments archéologiques. On peut faire l’hypothèse que la phase de pré-
domestication dans le Sud du Zagros et dans le Plateau Central Iranien. En effet, des
haplotypes identiques à ceux de cette région se retrouvent à plusieurs milliers de
kilomètres, ce qui est inhabituel chez les animaux (excepté chez les oiseaux ; e.g. Ball et
al. 1988 ; Questiau et al. 1999). Il est donc probable que les hommes aient transporté des
animaux dès la phase de pré-domestication, à partir de cette région (Sud Zagros, Plateau
Central Iranien) où la pré-domestication aurait été initiée (Figure 1.9).

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Figure 1.9. Région étudiée et distribution géographique des haplogroupes d’ADNmt pour
l’aegagres. a) Distribution naturelle du aegagre d’après Uerpmann (Uerpmann 1987). Les
sites archéologiques qui démontrent la domestication pré-Néolithique locale de chèvre
sont représentés en rouge. Les sites qui suggèrent la domestication locale de la chèvre, ou
le transfert de chèvres domestiquées au début de la période néolithique dite de « pré-
poterie », sont représentés en orange. Les sites qui fournissent l'évidence d’un transfert de
chèvres hors de la région géographique originelle de l’aegagre vers le milieu du 10 ème
millénaire Cal. B. P, sont représentés en jaune. b) Distribution géographique des
haplogroupes de mtDNA pour l’aegagre. La taille des cercles est proportionnelle au
nombre d'individus analysés. Les différents haplogroupes d’aegagre sont en codes
couleurs identiques à ceux utilisés pour la Figure 1.4. Les différentes localités identifiées
par des nombres, correspondent à celles décrites dans le tableau n°1 annexé à l’article n°2.

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La comparaison de la diversité génétique des aegagres sauvages avec celle des

chèvres domestiques et l’estimation du nombre d’haplotypes ancestraux capturés lors de la
domestication convergent pour montrer que la phase de domestication effective a aussi
concerné un grand nombre d’individus. Plusieurs dizaines voire centaines d’haplotypes
mitochondriaux ont très probablement été capturés. Cela n’a pu se faire qu’à une vaste
échelle géographique à partir des troupeaux sauvages prédomestiqués. Il est clair que
contrairement à ce qui a été démontré chez plusieurs plantes, la chèvre n’a pas subi de fort
goulot d’étranglement pendant sa phase de domestication.
La localisation des zones impliquées dans la phase de domestication effective est
possible en recherchant les populations sauvages actuelles présentant les génotypes les
plus proches des chèvres domestiques. En ce qui concerne l’haplogroupe domestique le
plus représenté (groupe A), l’origine le plus probable est l’Est de l’Anatolie qui serait donc
un centre de domestication. La présence d’haplotypes du groupe A au sud-est de l'Iran
serait plus vraisemblablement due à des introgressions à partir des domestiques. La
répartition géographique des haplotypes sauvages proches des autres haplogroupes
domestiques montrent qu’en plus de l’Est de l’Anatolie, le Zagros (Sud et Centre) serait
aussi impliqué dans la phase de domestication. Toutes ces conclusions concordent avec les
données archéologiques. Il est possible que ces différents évènements se soient produits à
différents moments entre 10 000 et 7 000 ans. Quoi qu’il en soit, nos résultats ne
soutiennent pas l’hypothèse d’un centre de domestication de la chèvre dans la basse vallée
de l’Indus.
Le scénario de la domestication de la chèvre que nous proposons remet donc en
question plusieurs hypothèses admises jusqu’à présent. La domestication se serait faite à
une vaste échelle géographique, sans doute sur une longue période de temps et en deux
étapes. La première étape, la pré-domestication, aurait consisté en une gestion durable des
troupeaux sauvages et avec des premiers déplacements d’animaux par l’homme. La
seconde étape, la domestication effective, aurait aussi concerné un grand nombre
d’individus d’où une absence de fort goulot d’étranglement permettant de capturer une
grande partie de la diversité génétique sauvage. Ces résultats soulèvent maintenant la
question de la généralisation de ce type de scénario, et notamment de l’existence d’une
phase de pré-domestication et l’absence de goulot d’étranglement, chez les autres animaux
domestiques.

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Article 3. Les vaches, les moutons et les chèvres sont-elles des espèces
menacées?

Ce chapitre est basé sur l’article “Are cattle, sheep, and goats endangered species?”
de P. Taberlet, A. Valentini, H.R. Rezaei, S. Naderi, F. Pompanon, R. Negrini, P. Ajmone-
Marsan publié dans Molecular Ecology (2007, doi: 10.1111/j.1365-294X.2007.03475.x)

Depuis une dizaine de milliers d’années, les fermiers ont géré les vaches, les moutons
et les chèvres de façon durable, ce qui a abouti à des cheptels bien adaptés aux conditions
locales dans lesquelles ils sont élevés. Il y a environ 200 ans, la situation a commencé à
changer dramatiquement avec la montée en puissance du concept de race. Tous les
animaux d’une même race ont commencé à être sélectionnés pour exprimer des traits
phénotypiques communs. Ainsi, la reproduction entre individus de races différentes a
fortement décliné, conduisant à une forte fragmentation des populations initiales.
Depuis quelques décennies les pressions de sélection ont encore augmenté avec
l’objectif d’augmenter la productivité, sans que la préservation de la diversité génétique
globale ne soit suffisamment prise en compte. Si l’efficacité des méthodes modernes de
sélection a permis une augmentation des rendements de production animale, elle a
également eu pour effet une diminution alarmante de la variabilité génétique. De
nombreuses races industrielles sont maintenant fortement consanguines avec des tailles
efficaces de populations inférieures à 50. Avec le développement de ces races, les éleveurs
subissent de plus en plus des pressions économiques les conduisant à abandonner leurs
races traditionnelles. Cela a déjà eu pour conséquence la disparition récente d’un grand
nombre d’entre elles. Ainsi, les ressources génétiques d’animaux d’élevage tels que la
vache, le mouton et la chèvre sont fortement menacées, essentiellement dans les pays
développés.
Il nous apparaît donc essentiel de promouvoir des mesures conduisant à une gestion
durable des ressources génétiques. Il faut avant tout préserver in situ les races menacées. Il
est aussi nécessaire de mettre en place des programmes de sélection afin de restaurer la
diversité génétique des races industrielles. Enfin, il est indispensable de protéger les
espèces sauvages proches des espèces domestiques qui peuvent devenir une ressource
génétique très utile.

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Conclusion

Depuis le début de la domestication, les processus démographiques, les mutations, la

dérive génétique, l’adaptation locale, et la sélection des races ont façonné la diversité
génétique des populations domestiques. Une bonne connaissance de la structure génétique
des populations domestiques et sauvages est donc essentielle pour comprendre l’histoire
de la domestication, mais aussi pour mettre en place des programmes de conservation.
Cela a été le cadre du travail que nous avons mené sur la chèvre domestique (Capra
hircus), l’un des premiers ongulés domestiqués il y a plus de 10 000 ans dans le Croissant
Fertile. L’histoire de la domestication a été abordée par l’analyse comparée de la diversité
génétique des chèvres domestiques et de celle de son ancêtre sauvage (Capra aegagrus).
Nous avons tout d’abord mis au point une méthode standard permettant d’établir une
nomenclature claire des haplogroupes mitochondriaux, et aussi de définir de nouveaux
haplogroupes lorsque cela s’avère pertinent. Cette méthode a été utilisée pour analyser
2430 séquences d’ADN mitochondrial (fragment HV1 de la région de contrôle), incluant
946 nouveaux échantillons issus de régions très peu étudiées jusqu’ici (notamment le
Croissant Fertile). Cinq des six haplogroupes mitochondriaux présentent une forte
diversité génétique, mais la diversité est essentiellement distribuée entre haplogroupes au
sein des régions géographiques. Cette faible structure phylogéographique résulterait
surtout de l’ubiquité de l’haplogroupe A (plus de 90% des chèvres), mais aussi de la vaste
répartition des autres groupes, conséquence très probable des migrations humaines.
Même avec un jeu de données aussi important que celui analysé ici, il est très
difficile de comprendre l’histoire de la domestication en se basant uniquement sur
l’analyse des animaux domestiques. Par exemple, il est difficile d’estimer précisément si
les expansions démographiques dont on voit la signature génétique sont antérieures ou
postérieures à la domestication. De plus, il n’est pas possible d’identifier le(s) centre(s) de
domestication de la chèvre à cause de la faible structure phylogéographique observée. On
n’identifie aucun gradient de diversité, alors que l’on attend une diversité décroissante à
partir du centre de domestication. Enfin, les données génétiques sur les domestiques seuls
ne permettent pas de tester précisément l’hypothèse d’un goulot d’étranglement au
moment de la domestication. C’est l’étude conjoint des ancêtres sauvages (les aegagres) et
des chèvres qui a apporté les nouvelles informations permettant de reconstituer l’histoire
de la domestication. Ces nouvelles informations concernent la localisation spatiale des
aegagres génétiquement proche des chèvres domestiques, la comparaison de la diversité

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nucléaire et mitochondriale des domestiques et des sauvages, et la reconstitution des

processus démographiques passés chez les aegagres. Ces données ont été acquises à partir
d’un échantillonnage extensif composé de 487 aegagres issus de 43 localités recouvrant
l’ensemble de l’aire de répartition de l’espèce. Elles ont permi d’établir un nouveau
scénario de domestication de la chèvre en deux étapes. La première étape correspond à une
phase de gestion des troupeaux sauvages par l’homme qui précède la domestication sensu
stricto. Pendant cette phase de pré-domestication, les troupeaux d’aegagres concernés ont
subi une expansion démographique dont la signature génétique est toujours visible
actuellement. L’estimation des paramètres démographiques montre en effet un taux de
croissance démographique plus fort chez les aegagres génétiquement proches des chèvres
que chez les aegagres d’haplotypes très divergents des domestiques. L’étape suivant la
pré-domestication est la domestication sensu stricto réalisée à partir d’individus issus des
troupeaux gérés par l’homme.
Les aegagres génétiquement proches des chèvres sont actuellement répartis sur une
vaste zone qui inclut l’Est de l’Anatolie, l’ensemble du Zagros, le Plateau Iranien Central
et le Nord Est de l’Iran. Cette distribution démontre que les phénomènes de pré-
domestication et de domestication ont été réalisés à grande échelle du point de vue
géographique. Ils ont également été de grande ampleur du point de vue génétique.
L’analyse comparée de la diversité nucléaire et mitochondriale chez les chèvres et les
aegagres démontre qu’une grande partie de la diversité génétique sauvage a été capturée
par les domestiques. Il n’y a donc pas eu de goulot d’étranglement au moment de la
domestication de la chèvre. Ce scénario est très différent des modèles précédents qui
mettaient en avant des phénomènes se produisant à une échelle réduite, avec des centres de
domestication très localisés et de fortes réductions de la diversité génétique.

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Perspectives

L’utilisation plus poussée de marqueurs nucléaires devrait permettre de mieux

comprendre l’histoire de la domestication. Le séquençage de nombreux gènes nucléaires
apporterait une masse d’information permettant d’estimer de façon fiable les dates
d’expansion des aegagres génétiquement proches des chèvres. Une expansion
démographique des aegagres antérieure à celle des chèvres domestiques confirmerait
l’existence de la phase de pré-domestication.
L’étude d’échantillons de chèvres issus de sites archéologiques apporterait également
des éléments nouveaux. La comparaison d’échantillons anciens et actuels devrait
permettre d’identifier des mutations expliquant les variations phénotypiques apparues et
sélectionnées pendant le processus de domestication, conduisant ainsi à l’identification des
gènes de la domestication.
Il paraît enfin nécessaire de tester si des scénarii de domestication à grande échelle
comme celui que nous avons pu mettre en évidence chez la chèvre sont plausibles chez
d’autres animaux domestiques. En d’autres termes, il s’agit de tester si l’absence de goulot
d’étranglement au moment de la domestication est nécessaire pour garantir le succès d’une
domestication animale durable.

Figure 1.10. Capra aegagrus à Malayer, zone protégée en Iran (Photo par HR. Rezaei).

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Chapter 2. Introduction
Chapter 2 Introduction

Chapter 2. Introduction

We are becoming more and more aware of the importance of the world’s biodiversity
– the variety of its plants, animals and micro-organisms, and of the ecosystems in which
they live. For a sustainable management of these genetic resources, we need at first to
know the evolutionary history of the organisms. The present structure of the genetic
diversity retains the signatures of past demographic events and helps to reconstitute the
evolutionary history (Luikart et al. 2003). Nature and human impacts are the most
important forces that always affected the evolutionary history of organisms. One of the
most important human impacts on organisms is the domestication process (Pääbo 1999). A
few wild species became domesticated. The precise analysis of the genetic structure of
both wild and domestic species can provide invaluable data to track and understand the
domestication process itself.
Beside the wild ancestor when it still exists, the different domestic breeds can be
considered as genetic resources. Breeds with the highest genetic diversity represent the
most valuable resources, and are expected to be found close to the domestication centres
(Bruford et al. 2003). As a consequence, the precise knowledge of wild ancestors, of
domestication centres, and of colonization routes is of prime importance for tracking
genetic resources (Zeder et al. 2006a).
The 40-plus livestock species contributing to today’s agriculture and food production
are shaped by a long history of domestication and development. Selection pressures
resulting from environmental stress factors, and the controlled breeding and husbandry
imposed by humans, have been combined to produce a large variety of genetically distinct
breeds. This diversity, developed over thousands of years, is a valuable resource for
today’s livestock keepers. Genetically diverse livestock populations provide a greater
range of options for meeting future challenges, whether associated with environmental
change, emerging disease threats, new knowledge of human nutritional requirements,
fluctuating market conditions or changing societal needs (FAO 2007).
If the domestication process was the major initiating event in the development of
today’s livestock diversity, the subsequent dispersion and migration of domesticated
species across all five continents was equally important. This process played a major role

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in the emergence of the current geographic distribution of livestock diversity. The main
factors at the root of the early dispersion of livestock species were the expansion of
agriculture, trade, and military conquests. This resulted in genetic (e.g. selection, gene
flow) and demographic processes that explain the present worldwide distribution
(Diamond 2002). After the initial plant and animal domestications in the Near East, ca.
11,500 and 10,500, respectively, years ago (ya) (Harris 1996), Neolithic culture diffused
into Europe along two main routes: ‘‘Mediterranean” route and ‘‘Danubian’’ route
(Diamond & Bellwood 2003).
From the beginning of animal husbandry in prehistory to the mid-twentieth century,
gene flow generally enhanced diversity. However, during the past five decades the
development of intensive selection to increase the production led to a reduction in
diversity. Furthermore, the large-scale replacement of local breeds with a small number of
globally successful breeds also contributed to a strong overall diversity in domestic breeds.
This process was particularly intense in North America and Europe, where 50 percent of
documented breeds are classified as extinct, critical or endangered. It is now being
replicated in developing countries, and represents a major threat to the conservation and
utilization of indigenous animal genetic resources (FAO 2007).
Clarification of the geographic pattern and history of the dispersal of livestock is
essential to the identification of original geographic areas with high levels of diversity,
which are potential priority areas for conservation efforts. This requires extensive mapping
of genetic diversity. Thus, if distant livestock populations are relatively similar
genetically, we can infer that humans transported animals. Up to now, very few studies
have been undertaken in this field.
In summary, the combined effects of portability/mobility on the one hand (goats and
horses) and introgression on the other (cattle, sheep and pigs) has shaped the distribution
of genetic diversity that we see in livestock on a global scale today (Bruford et al. 2003).
How gene flow will impact diversity in the future will depend primarily on the policy and
legislative frameworks that are now in the process of being developed. It seems likely that
the transfer of livestock selection programs will continue and even increase rapidly in
developing countries. The crowding out of locally adapted breeds will probably accelerate
in many developing countries, unless appropriate support is given to local livestock
keepers for promoting in situ conservation.
It is critical that the analysis of the domestication history be conducted with not only
an appreciation of the biology of domesticated plants and animals, but also with an

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Chapter 2 Introduction

understanding of the cultural context of the human partners in the process. And this is
where genetics and archaeology come together to provide a richly detailed understanding
of domestication (Zeder et al. 2006a). As the origin and diffusion of livestock is intimately
linked to human evolution and migrations, data from domestic goats, sheep, cattle and
other species can be used as a way to study the history of human populations (Fernández
et al. 2006).

1. Tools to understand livestock origin and diversity

1.1. Genetic tools

Genetic tools have a central role in many biological investigations. For instance,
genetic analysis can provide insights into diverse investigations such as evolutionary
histories of species (Avise et al. 1987), interactions and relationships among populations
(Luikart et al. 2001; Meadows et al. 2007), or individuals (Queller et al. 1993), evaluation
of the success of specific management actions and conservation (Manceau et al. 1999b ;
Vernesi et al. 2002), population and behavioral ecology (Scribner & Chesser 2001) and
food habits (Symondson 2002). DNA-based markers have been developed since the 1970s
(Karp et al. 1997; Sunnucks 2000) but have only been actively applied to studies of animal
domestication and diversity since the early 1990s (Loftus et al. 1994).
A series of recent genetic studies has revealed the remarkably complex picture of
livestock domestication. By comparing mitochondrial (mtDNA) and nuclear DNA
sequences of modern breeds with their potential wild ancestors, we have gained new
insights into the timing and location of domestication event(s) that produced the farm
animals. Recognizing of real number of domestication events and the locations in which
they took place are very important for determination of our approach to conserving
livestock biodiversity resources in the future (Bruford et al. 2003).

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1.1.1. Choosing molecular markers

To help understand the origins of domestication of a livestock species, the ideal

molecular marker should have several characteristics. First, it should be sufficiently
conserved to allow the identification of the wild taxon or population from which the
species descends. Second, the marker should be variable and structured enough across the
geographical range of the wild ancestor so that the approximate locality of domestication
can be identified. Third, the marker should evolve at a rapid but constant rate — this
feature allows the origin of a particular polymorphism to be dated. This combination of
characteristics is difficult to find, but fortunately, in animal evolutionary studies, there is
such a marker: mtDNA. At present, mtDNA is by far the most widely used molecular tool
in domestication studies (Bruford et al. 2003).
Protein polymorphisms were the first molecular markers used in population studies.
A large number of studies, particularly during the 1970s, documented the characterization
of blood group and allozyme systems. However, the level of polymorphism observed in
proteins is often low, which reduces the general applicability of protein typing in diversity
studies (Randi et al. 1990).
DNA-based polymorphisms are now the markers of choice for molecular-based
surveys of genetic diversity. Many genetic studies of plant and animal domesticates do not
focus on the particular genes responsible for the changes in morphology, behavior, and
physiology that distinguish domesticates from their wild progenitors. Instead, these studies
generally concentrate on variation in neutral genes or in non-coding genetic regions that
can be used to trace the evolutionary history of domesticates and their wild progenitors
(Zeder et al. 2006a).

1.1.2. Mitochondrial DNA

Mitochondrial DNA is a small DNA molecule (less than 20 kb in most mammals)

that is located only in mitochondria. It is the most widely used DNA marker for studies of
closely related populations such as domestic breeds. Especially the highly variable section
of this molecule, the control region, has a rapid rate of evolution, which leads to a high
level variability within species. It represents an ideal marker for studying the divergence
between wild and domestic populations under a relatively short time scale over which
domestication operated (Zeder et al. 2006a). For instance, in a study of the control region

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Chapter 2 Introduction

diversity in domestic goats (Capra hircus), 331 haplotypes were identified from 406
individuals (Luikart et al. 2001). The lack of recombination associated with exclusive
maternal inheritance allows the identification of maternal lineages that have diverged
through time only via accumulation of new mutations. Moreover, the presence of mtDNA
at a high copy number in most cells facilitates its extraction from ancient material, thus
making it very suitable for archaeological genetic studies (Fernández et al. 2005).
Also this marker is less sensitive to introgression from wild species than nuclear
DNA. Nuclear gene histories may have been complicated through more ephemeral
encounters between wild males and tame females (Bruford et al. 2003). Since the effective
population size of mtDNA is one-quarter that of nuclear DNA, it has proven particularly
useful in the study of population dynamics because it is capable of detecting population
bottlenecks that are likely to occur in domesticates, but which have less impact on nuclear
DNA (Zeder et al. 2006a). For interspecific studies the mtDNA cytochrome b gene (cyt b)
is more appropriate than the control region because it evolves less rapidly, being under
functional constraint as a coding gene. Thus, it is easier to align between species (without
sequence gaps) and, in conjunction with the fossil record to calibrate a molecular clock,
easier to use for estimating divergence dates between taxa (e.g., sheep and goat diverged -
6 MYA) (Luikart et al. 2006).
In summary, mtDNA sequences are the markers of choice for domestication studies.
More specifically, mtDNA sequences are used to identify putative wild progenitors, the
number of maternal haplogroups and their geographic origins. It can also be used to track
geographic patterns of diversity and evolution (phylogeography). Mitochondrial DNA can
also tell us about the recent demographic processes affecting a population, for example
whether a population has undergone a recent demographic expansion, or has a more
complex history (Bruford et al. 2003).

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Chapter 2 Introduction

Figure 2.1. Schema of the Mammalian mitochondrial genome

However, there are some limitations. Mitochondrial DNA can be a poor predictor of
overall genomic diversity, because it behaves like a single locus and is an extra-nuclear
genetic marker with specific evolutionary dynamics. Crucially, as it is maternally
inherited, mtDNA does not detect male mediated gene flow, which has had a powerful
influence on the evolution of livestock species in modern times. Thus, although nuclear
DNA is less variable than mtDNA in animals and therefore generally less useful in
phylogenetic studies of relatively shallow time depth, studies on nuclear genes are needed
because they give information on gene flow and selection processes that had a great
influence on the evolution of livestock species (MacHugh et al. 1997).

1.1.3. Amplified fragment length polymorphism (AFLP)

This multilocus marker screens many loci distributed randomly throughout the
genome, simultaneously. This is a relatively cheap, easy, fast and reliable technique based
on DNA fingerprinting that detects hundreds of informative genomic restriction fragments
by PCR amplification (Mueller & Wolfenbarger 1999). Fingerprints are produced without
prior sequence knowledge using a limited set of generic primers. The number of fragments
detected in a single reaction can be 'tuned' by selection of specific primer sets. The

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Chapter 2 Introduction

technique will display presence or absence of restriction fragments rather than length
differences. In general, there is an almost linear correlation between numbers of amplified
fragments and genome size (Vos et al. 1995).
AFLP markers have proved useful for assessing genetic differences among
individuals, populations and independently evolving lineages, such as species. Because of
the rapidity and ease with which reliable, high-resolution markers can be generated,
AFLPs are emerging as a powerful addition to the molecular toolkit of ecologists and
evolutionary biologists (Ajmone-Marsan et al. 2001), and increasingly used in plant and
animal domestication studies (Bruford et al. 2003).
The main disadvantage of AFLP markers is that they show a dominant mode of
inheritance, i.e. heterozygotes cannot be characterized. This reduces the power of
population genetic analyses, which generally require more informative codominant
markers allowing heterozygosity analyses (Bruford et al. 2003).

1.1.4. Y-chromosome DNA

This DNA marker is transmitted by males only, without recombination. It is

especially useful for reconstructing paternal lineages, and thus represents the "male view"
of evolutionary history. Information from Y-chromosome is complementary to mtDNA
data, although its DNA sequences are generally far less polymorphic, and therefore less
informative (Luikart et al. 2006; Hanotte et al. 2000). The nucleotide diversity present on
the mammalian Y-chromosome appears generally lower than that found on autosomes
(Hellborg & Ellegren 2004). Information from the Y-chromosome is likely to be
particularly important in domestic animals where the contribution of a small number of
males has been disproportionately large during breed development, leading to a reduction
of the polymorphism. In addition, examination of the Y-chromosome has the capacity to
reveal the identity of those wild ancestors at the origin of the domestic breeds (Meadows
et al. 2004). However, the possibility of paternal gene flow from wild males that mate
with domestic females might have a confounding effect (Luikart et al. 2006). In case of
hybridization between different breeds, the analysis of Y-chromosome polymorphism
might allow to detect and to quantify male-mediated admixture (Hanotte & Jianlin 2005).

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Chapter 2 Introduction

1.1.5. Microsatellites

Simple sequence repeats (SSR), also known as microsatellite repeats, consist of short
nucleotide sequences (e.g. CAT) that are repeated many times in tandem
(…CATCATCAT…). SSR are codominantly inherited. The number of SSR tandem
repeats can vary in a sequence, and many such variants (alleles) can exist in a population.
The repeated sequences is often simple, consisting of two, three or four nucleotides (di-,
tri- and tetranucleotide repeats, respectively), and can be repeated 10 to 100 times. As
there are often many alleles present at a microsatellite locus, the origin of a particular
allele can be identified, provided that the pedigrees are known (Goldstein et al. 1995).
Microsatellites are the most useful DNA markers for measuring and comparing levels
of diversity (e.g., number of alleles) within populations because these markers are highly
variable, often having 5-10 alleles per locus. The analytical strengths of microsatellite
markers are co-dominance and hypervariability (Queller et al. 1993). These markers can
thus be used to compare levels of diversity within populations from different continental
regions (e.g. inside and outside the centres of domestication). Microsatellites can also be
useful for assessing genetic relationships among closely related populations (isolated for
only several dozen generations) (Luikart et al. 2006).
Microsatellites have three primary uses in domestication studies. First, they can be
used to quantify genetic variation within and among livestock populations or breeds.
Second, they allow the documentation of admixture (genetic mixing) among livestock
populations. Third, microsatellite data can be used to assign individuals to genetically
similar groups at the population, breed or species levels. Microsatellites markers are also
highly sensitive to genetic bottlenecks and selection, both of which are likely to have
occurred during domestication events (Bruford et al. 2003).
Microsatellites also have some limitations. This type of marker developed for a
particular species can often be applied to closely related species, but the percentage of loci
that successfully amplify may decrease with increasing genetic distance. In other words,
microsatellite primers developed for one species can rarely be used beyond the very
closest relatives. Furthermore, the risk of null alleles (non-amplifying alleles) increases
when the primer sequences were not designed specifically for the species under study.
Therefore, it is better to develop microsatellite markers for each species. Finally, the

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Chapter 2 Introduction

implementation of a microsatellite study is technically demanding, and the development is

time-consuming and expensive (Jarne & Ladoga 1996).
The molecular markers used to characterize diversity in livestock have up to now
little to do with the genes under selection for economically important traits. The
identification of causative mutations for phenotypic variation will add a new dimension to
the characterization of animal domestication, as it will allow researchers to trace selection
and the spread of economically important alleles. Such analysis is potentially very
powerful, especially when combined with single nucleotide polymorphism (SNP)
screening methods, and indicates that there are exciting new avenues of research in this
area. With the publication of genome sequences for key domestic species (for example for
cattle genome see in: [Link] and for chicken
genome see in: [Link] ) and the increasing
availability of expressed sequence tag (EST) databases, we can expect an exponential
increase in the availability of both neutral and selected markers. It is exciting that in the
future we should be able to simultaneously detect male and female demographic history
and the signatures of selection, past and present, within the genomes of our domestic
livestock (Bruford et al. 2003).

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Chapter 2 Introduction

1.2. Archaeobiological approaches

Advances in molecular genetic and archaeobiological techniques in the

interdisciplinary investigations over the past two decades have resulted in a virtual
explosion of studies exploring the origins of plant and animal domestication.

1.2.1. Ancient DNA

It appears necessary to complete the analysis of the modern DNA diversity with
ancient DNA (aDNA) studies that can potentially facilitate our understanding of the origin
and the routes of diffusion of domestic species. This is feasible through both research of
the DNA diversity of the wild progenitors just before the earliest domestication, and by the
analysis of the evolution of the DNA diversity of domestics through times. In fact, ancient
DNA provides a tremendous opportunity for the integration of archaeology and biology in
the study of plant and animal domestication (Fernández et al. 2005).
Ancient DNA studies could be particularly helpful in pinpointing the site of
domestication. For example, evidence for a local domestication would be provided by
finding a DNA haplogroup in ancient domestic animals from one location (e.g., the Fertile
Crescent) but not from other locations (e.g. East Asia). Even more compelling would be
the discovery of a unique DNA haplogroup in both wild and domestic animals from one
location, but a different DNA haplogroup in the wild and domestics from another location.
Moreover, distinguishing between local domestication versus introgression might be
facilitated by using ancient DNA samples from wild and domestic animals sampled
through time (e.g. 12,000 to 5,000 years ago) in regions where domestication likely
occurred (Luikart et al. 2006).
However, there are limitations in the utilization of aDNA in domestication studies.
DNA is poorly preserved in warm climates corresponding to the putative centres of
domestication. Up to now, no aDNA was recovered from bones of animal dating to the
earliest phases of the domestication process, but a few studies analyzed more recent
samples from European sites (Fernández et al. 2006; Larson et al. 2007). However, we can
expect that future studies of aDNA combined with archaeozoology, will likely yield new
discoveries greatly advancing our understanding of the origin and spread of farm animals
and their role in ancient human societies. It will also be possible, for domesticated

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Chapter 2 Introduction

animals, to track the timing of genetic change along with that of the other non-
morphological and morphological indicators domestication (Zeder et al. 2006a).

1.2.2. Archaeological markers

The archaeological markers may take the form of morphological change in the target
species, changes in its genetic structure, a restructuring of its population biology, or the
transformation of its ecological context. Markers of domestication may also be found in
the tools, settlement patterns, or even the ideology of the human partners in the
domestication process (Zeder et al. 2006).
The archaeological markers for animal species domestication studies can be divided
into two categories: 1- Morphological markers 2- Nonmorphological markers

[Link]. Morphological Markers

[Link].1. Genetically driven markers

Those are that reflect genetically driven, selective responses to domestication passed
from one generation to the next. These markers reflect the evolutionary impact of
domestication on the animal on a population level (Animal-oriented markers). The
domestic animals display a set of changes in behavioral, physiological, and morphological
characteristics that can be directly tied to selection for less aggressive behavioral traits,
such as earlier onset of sexual maturity and more frequent receptivity, smaller brain size
and other changes in neurological organization, shortening of the snout, tooth-size
reduction and changes in tooth number, the changes in the size and shape of horns, smaller
bodies, and lessening of sexual dimorphism (Zeder 2006b).
Clearly, beside of domestication there are a number of other factors that may cause
morphological changes in organisms. The impact of these factors will also vary depending
on the biology of different species and the nature of their interaction with humans. For
example change in body size is the most widely used marker of animal domestication
today. But, there are other factors that affect body size in both wild and domestic species
that have nothing to do with domestication (e.g., sexual dimorphism, age, geography and
climate changes and habitat destruction)(Zeder 2006b). Most importantly, the cause and
effect mechanisms that link domestication to body-size reduction are still less than

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Chapter 2 Introduction

adequately known (Zeder 2006c). Such morphological changes, if related to the process of
domestication at all, are only delayed, and possibly indirect, artifacts of human
management (Zeder et al. 2006).

[Link].2. Plastic Responses to domestication

These markers operate on individual animals and will vary in degree and nature
depending on highly localized factors that may change over time. A beveling on the lower
second premolars of horses in the Eurasian steppe has been interpreted as definitive
evidence of bit wear and therefore domestication (Brown & Anthony 1998). Recently, a
number of researchers have begun to explore the potential of dietary shifts as detected by
isotopic analysis as a marker of initial domestication in animals (e.g., Balasse et al. 2000,
for sheep and goats). Again, it is important to remember that dietary conditions of early
domestic animals will vary depending on the environment in which they are raised and the
management practices used by their human masters. Therefore, it would be a mistake to
attempt to apply any single isotopic or other chemically detected shift in diet as a
definitive marker of domestication in any species in any single region, and certainly not as
a widely applicable marker across species and regions (Zeder 2006b).

[Link]. Non-morphological Markers

These markers seek to detect evidence of human management or control of animals

(Human-oriented markers), especially those that may precede any detectable, genetically
driven morphological change (Zeder 2006b).

[Link].1. Demographic profiling

Demographic profiling was one of the first of non-morphological markers that has
been applied to animal domestication studies. The technique is based on the assumption
that the age and sex of animals taken by hunters interested in maximizing the return from
their hunt will differ from the age and sex of those harvested by herders interested in
promoting the long-term growth of their herds. The demographic profiling, particularly
sex-specific harvest profiles, constructed by combining osteometric data and precise
radiocarbon dating (using accelerator mass spectrometer; AMS), are capable of

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Chapter 2 Introduction

distinguishing between herd management and a range of selective and non-selective

hunting practices (Zeder 2006c). However, this method has limitations in the techniques
used to reconstruct these profiles. Most importantly, until recently, it has not been possible
to construct separate harvest profiles for male and female animals, which is essential in
order to distinguish certain hunting practices from herding (Zeder 2006b).

[Link].2. Zoogeography and abundance

The appearance of a potential domestic species outside its presumed natural range is
often taken as a signal of human involvement in the movement of animals, either as
already domesticated herds or as captive wild animals undergoing domestication. The
zoogeographic data can sometimes be problematic in making the case for animal
domestication. Without direct dating, it is difficult to know if a specimen is contemporary
with the strata in which it was found or with a later intrusion into earlier strata (Zeder
2006b).
Moreover, present-day distributions of wild progenitor species have been strongly
affected by over-hunting and by the loss of habitat due to agriculture and urban settlement.
Past distributions are therefore likely to be quite different today from what they were
during the Early Holocene. The use of relative abundance data to mark initial stages of the
domestication process faces similar problems, especially in assemblages from sites within
or close to the likely natural habitat of wild progenitors. Without additional evidence of
domestic status (i.e. morphological change or domestic demographic patterns), it is
difficult to tell if an increase in the use of a potential domestic species signals the adoption
of herd management or the intensification of hunting strategies (Zeder 2006c).

[Link].3. Different types of more circumstantial evidence of human control

Remnants of pens or corrals, sometimes with associated dung pellets, have been used
as evidence for domestication. The architectural features (i.e. corals and other animal
shelters), artefacts associated with the use of animal resources (i.e. chums or milk
strainers), and artistic renderings that feature domesticates or herding activities (Zeder
2006b).

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Chapter 2 Introduction

There is no single prescription for animal domestication studies that can be

universally applied to all species in all regions. Instead, researchers need to choose the
best methods according to both the species and the cultural context that they face.
Combining genetic and archaeological information provides the most fruitful approach for
unlocking the secrets of the origins of domestic animals. Determining the time and
location of origin of ancient genetic lineages can be best done using reliably dated fossils
from archaeozoologists. Similarly, tracking the diffusion of these different genetics
lineages requires well-dated fossil material from each of several archaeological sites
(Luikart et al. 2006).
Also, with intraspecific study of genetic variation, linkages with other types of data
are needed. These other attributes include geography, morphology, and ecology. The
partnering of these varied sources of information with genetic variation falls into the
emerging field of phylogeography, where aspects of the past of an organism are read from
modern distributions of phylogenetically related sequence variants. Phylogeography has
been described as a subject with two orthogonal dimensions: the horizontal one of the
geography of genetic diversity and the vertical one representing the time through which
this geography emerges (Avise 2000). Therefore, the study of domestication must follow
an interdisciplinary approach (Bradley 2006).

2. Livestock biodiversity

2.1. Current knowledge

2.1.1. Species diversity

Mutation, selective breeding, and adaptation have shaped the diversity of livestock
populations. Only about 40 of the 50,000 known avian and mammalian species have been
domesticated. On a global scale, five species – cattle, sheep, chickens, goats, and pigs –
show widespread distribution and particularly large numbers. The first three are the most
widely distributed domestic species globally, while the latter two are less evenly spread
(Figure 2.2). Goats are much less numerous in the Americas, Europe and Caucasus than in
other regions (FAO 2007).

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Chapter 2 Introduction

Figure 2.2. Global distribution of five major domestic species: cattle, sheep, chickens,
goats, and pigs.

2.1.2. Breed diversity

Definition of breed adopted by FAO

Either a subspecific group of domestic livestock with definable and identifiable
external characteristics that enable it to be separated by visual appraisal from other
similarly defined groups within the same species or a group for which geographical and/or
cultural separation from phenotypically similar groups has led to acceptance of its separate
identity (FAO 1999).

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Chapter 2 Introduction

The total number of breed records in the Global Databank has increased greatly since
the publication of the World Watch List for Domestic Animal Diversity (WWL–DAD: 3,
Scherf 2000).

Table 2.1. Status of information in the Global Databank for Animal Genetic Resources
(FAO 2007).

A global total of 7 616 breeds have been reported. Europe and the Caucasus, and
Asia are home to the largest share of breeds of most of the world’s major livestock
species. Camels are the exception, with the largest number of breeds being found in
Africa. In terms of population size, Asia is the dominant region for most species.
Exceptions include camels (Africa), turkeys (Europe and the Caucasus) and horses (44
percent of which are found in Latin America and the Caribbean) (FAO 2007).

Figure 2.3. Distribution of the world’s mammalian breeds by species

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Chapter 2 Introduction

2.2. Livestock’s genetic diversity

Overall, the level of mtDNA polymorphism in cattle, sheep, and goats is high, and
contains evidence of multiple maternal origins. Such multiple origins correspond either to
several domestication events in different locations and/or at different periods, or to the
capture of several mtDNA haplotypes during a single domestication event. Furthermore,
nuclear DNA polymorphism seems high (see e.g. Maudet et al. 2002), comparable to what
is found in wild species (Taberlet et al. 2007).

2.3. Goat and its general situation

The genus Capra, which contains domestic goats and their wild relatives (Bezoar,
Markhor, Spanish ibex, Alpine ibex, Nubian ibex, Walia ibex, East Caucasian tur, West
Caucasian tur and Siberian ibex) displays an old-world distribution. Fossil data suggest
that the Capra first appeared in Central Asia (Pilgrim 1947) and that a species radiation
occurred in the Plio-pleistocene (Pilgrim 1947; Hartl et al. 1990). Very few
paleontological data are available for species of this genus because their preferred
mountainous habitats are not favourable for fossil preservation. Consequently, the
evolutionary history of Capra species is poorly understood. This is compounded by the
fact that the radiation of Capra taxa apparently occurred rapidly (Hartl et al. 1990;
Manceau et al. 1999a), making it difficult to assess the number of species and their
phylogenetic relationships. The number and status of Capra species and subspecies is still
under debate, with estimates ranging from 6 to 9 species (Schaller 1977; Shackleton 1997;
Pidancier et al. 2006).
This species is most hardy of all livestock species and will thrive and breed on the
minimum of food and under extremes of temperatures and humidity. They can provide
with clothing, meat and milk as well as bone, sinew, dung and manure (Pringle 1998;
Clutton-Brock 1999). Goats were also easy to transport in boats over long distances, as
well as by land, following humans better than sheep or cattle. For these reasons, goats
were among the first farm animals domesticated and were important in the economies of
societies as long as 10,000 years ago (Clutton-Brock 1999; Zeder & Hesse 2000).
Subsequently, goats were taken along during human migrations and colonizations, and in
more recent times, on ships exploring new continents (Porter 1996).

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Chapter 2 Introduction

Goats are the least numerous of the five major livestock species. There are about 800
million worldwide – one for every eight people. Some 70 percent of the world’s goats are
in Asia and the Near and Middle East. Goat breeds contribute 12 percent to the total
number of recorded mammalian breeds in the world (FAO 2007).
Goats are of major economic significance for smallholders in the South, particularly
in ecologically marginal areas such as drylands and mountains, where other domestic
animals cannot easily be kept. They are of limited importance in Northern agriculture,
though some highly productive dairy breeds have been developed in central Europe
through upgrading local stock with dairy breeds of Swiss origin. Rising living standards in
the Near and Middle East and the migration of people who prefer goat meat, have
increased the demand for goat meat, furthering the spread of the Boer goat during the past
few decades (Alandia Robles et al. 2006).

2.4. Goat genetics diversity results, up to now

Up to now, 5 mtDNA haplogroups have been recognized based on different regional

and worldwide scale genetic studies. According these studies, most of the genetic diversity
occurred within breeds, and only about 10% of the total mtDNA variation was due to
differences among continents. This is far lower than the published estimates of 54-80% in
cattle for the same mtDNA region. This suggests that in the past goats were transported far
more extensively than cattle. The very weak geographic structure has been interpreted as
the result of the extensive transportation of goats among continents (Luikart et al. 2001;
Sultana et al. 2003; Joshi et al. 2004).
Interestingly, the percentage of mtDNA variation (HVI) between continents for
humans is surprisingly similar (10%) to that in goats. This similarity might be
coincidental, but it is intriguing to speculate that goats have had similar amounts of high
intercontinental movement because they have been more important during human
movements (migrations, colonizations) or more used in historical commerce and trade
than cattle (Luikart et al. 2006).
The molecular clock approach allows the time of divergence between haplogroups to
be estimated based on the fact that the mutation rate is approximately constant through
time. Since mitochondrial genes are not affected by environmental selection pressures, the
number of mutations is roughly proportional to time. In this way, using published sheep

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Chapter 2 Introduction

cytochrome b sequences and established dates based on fossil data for the split between
Capra and Ovis, Luikart et al. (2001) estimated the divergence time between these
haplogroups more than 200,000 years ago, well before the time of domestication. This
timeframe is much earlier than domestication, suggesting that the mtDNA in today's
domestic goats does not originate from within one local population only 10,000 years ago.
These highly divergent haplogroups could not have evolved (i.e., accumulated so many
mutations) in only 10,000 years. It is more likely that three genetic origins occurred from
three different wild populations that already carried quite distinct mtDNA 10,000 years
ago. This suggests that the wild progenitors of the three lineages probably belonged to
different populations of wild goats (Luikart et al. 2001).
Additionally, on the base of a restricted study, at least three distinct groups of
domestic goats were found based on Y-chromosome polymorphism (Pidancier et al.
2006). Interestingly, all individuals from a given divergent mtDNA lineage did not always
come from the same distinctive Y-chromosome lineage. This is not surprising, because of
the extensive gene flow among goat populations and regions, which is likely to mix
maternal and paternal lineages within and among breeds. In contrast to mtDNA, Y-
chromosome data seems to suggest a higher diversity in the Fertile Crescent region than in
other regions. For example, two Y-chromosome lineages were found in contemporary
goats from Jordan and Turkey, but not in other regions (Luikart et al. 2006).
The origin and spread routes of the different goat haplogroups across the Old World
was analyzed by Fernández et al. (2005), using 130 bp of the mtDNA control region of the
ancient DNA extracted from samples of archaeological sites in Europe and the Middle-
East. They found that several ancient samples from the prehistoric sites of the Qazvin
Plain in the northern part of the Iranian Central Plateau belong to A haplogroup, the main
haplogroup that was found worldwide in modern goats. In another study, Fernández et al.
(2006) were able to analyze several ancient samples from Europe (Southern France)
belong to the A and C haplogroups. But, none of other haplogroups have been found in
ancient sequences up to now.
An extensive survey to examine patterns of thirty microsatellites variation in 1426
domestic goats from 45 traditional or rare breeds in 15 European and Middle Eastern
countries, clearly indicates a geographical partitioning of goat diversity, with a large
proportion of the genetic diversity found among breeds. About 41% of the genetic
variability among the breeds could be explained by their geographical origin. A decrease
in genetic diversity from the south-east to the north-west was accompanied by an increase

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Chapter 2 Introduction

in the level of differentiation at the breed level. These observations support the hypothesis
that domestic livestock migrated from the Middle East towards western and northern
Europe and indicate that breed formation was more systematic in north-central Europe
than in the Middle East (Cañón et al. 2006).

3. Domestication

3.1. The domestication process in general

Domesticated animals are considered to be those species that are bred in captivity,
and modified from their wild ancestors to make them more useful to humans, who control
their reproduction (breeding), care (shelter, protection against predators) and food supply
(Diamond 2002; Mignon-Grasteau 2005). Domestication includes the following steps:
initial association with free breeding; confinement; confinement with breeding in
captivity; and selective breeding and breed improvement (Zeuner 1963).
At domestication time, at the end of the Pleistocene the climate had started to become
warmer and more seasonal, favouring plants with large roots and tubers and large seeded
annual plants. Such species are easy to harvest, cultivate and store and so are well suited to
farming. These species probably became increasingly important food resources during
seasons in which other food was unavailable. With the climatic reversal of the Younger
Dryas cold period (12,200–11,100 YBP), the demand for cultivated and storable food
increased and led to the domestication of species such as rice, wheat and legumes. As the
climate warmed, some human populations started expanding rapidly and population
centres became established in regionally important sites. Settlements tended to be located
in naturally fertile areas that were suitable for agriculture, or in locations that linked
different landmasses, and so were natural stopping-off points for migrating peoples
(Salamini et al. 2002). The indigenous population, together with migratory populations,
needed to be supplied with food, and this would have provided another stimulus for
farming and the domestication of agricultural species. From this time very few animal
species have been successfully domesticated. Domestication was a complex and gradual
process, which altered the behaviour and morphological characteristics of the ancestral
animals. The circumstances and pressures that affected the domestication of animals
remain uncertain, and may have varied from one geographic area to another and from one
species to another. But, it seems that the root of animal domestication is probably related

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Chapter 2 Introduction

to the ubiquitous tendency of hunter-gatherers to try to tame or manage wild animals. In

this situation, the main object of animal domestication may have been the desire to secure
the availability of “favourite” foods. The potential of some domesticated species to
provide support to crop farming (e.g. ploughing with oxen or buffalo), or as pack and
riding animals (e.g. llamas, dromedaries, Bactrian camels, horses, donkeys and even
cattle) being realized later (Diamond 2002).
Clearly there are some universal principles that come into play in domestication
process story, both cultural and biological. Climate, community, optimization, adaptation,
co-evolution, and selection all serve to shape the process of domestication wherever it
occurred. But there are other highly localized factors that play important roles in each
instance. Understanding what these factors are and how they shaped the unfolding process
of domestication are equally, perhaps even more, important in explaining domestication
(Zeder 2006).
Among the 148 non-carnivorous mammalian species weighing more than 45 kg, only
15 have been domesticated. Thirteen of these species are from Europe and Asia, and two
originate from South America. Moreover, only six species have become widespread on all
continents (cattle, sheep, goats, pigs, horses, and donkeys), while the remaining nine
(dromedaries, Bactrian camels, llamas, alpacas, reindeer, water buffalo, yaks, Bali cattle,
and mithan) are important in more limited areas of the globe (FAO 2007).

3.2. Domestication history

The history of animal domestication started around 12 000 to 14 000 years ago
during the agricultural revolution of the early Neolithic, with the domestication of major
crop and livestock species. The control of food production by early farmers led to major
demographic, technological, political, and military changes. The domestication of animals
and plants is considered to be one of the most important developments in history, and one
of the prerequisites for the rise of human civilizations (Diamond 2002). After the initial
domestication events, the spread of farming into nearly all terrestrial habitats followed
rapidly (Diamond & Bellwood 2003, Figure 2.4). During thousands of years, natural and
human selection, genetic drift, inbreeding and cross-breeding have contributed to today’s
animal genetic resources diversity and have allowed the development of sustainable

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Chapter 2 Introduction

livestock production in a variety of environments (agro-ecological zones) and production

systems (Bruford et al. 2003).

Figure 2.4. Archaeological map of agricultural homelands and spread of

Neolithic/Formative, with approximate radiocarbon dates (Diamond & Bellwood 2003).

However, based on molecular genetics and archaeological data, exact dating of

domestication events has proved to be particularly challenging. Animals undergoing the
initial process of domestication would not have been significantly different in morphology
from their wild ancestors, and dates relying on morphological characters will undoubtedly
underestimate the age of domestication events, because the expression of morphological
changes is often delayed in domestic animals (Zeder 2006; Dobney & Larson 2006). The
process of molecular dating, while independent of morphological changes, is typically
characterized by large confidence intervals, and often relies on uncertain calibration
points. In fact, the molecular-clock hypothesis is controversial in general, for any
timescale, taxon, or genome type. Even if one ignores the evidence for unequal mutation
rates among different groups and different genomes, the timescale of domestication is
much too short to be appropriate for molecular clocks, which are better calibrated for
species that diverged millions or tens of millions of years ago, not populations (such as
domesticates) diverging thousands of years ago (see Ho et a1. 2005; Ho & Larson 2006;
Ho et al. 2007).

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Chapter 2 Introduction

Approaches including demographic profiling techniques for identifying initial

attempts at livestock management by humans, and calibration of molecular clocks using
ancient DNA information, are providing new approaches for pinpointing the dates of
domestication. However, the precise dating of domestication events might come from the
genetic analysis of fossil bones properly dated by archaeozoologists (Zeder 2006).

3.3. Domestication centers

Livestock domestication is now thought to have occurred in at least twelve areas of

the world. Interestingly, not all centres of domestication are closely associated with the
homelands of our crop species. While in some cases (e.g. the Fertile Crescent),
domestication centres of both crops and livestock are intermingled, in others (e.g. the
African continent) crop and livestock domestication seem largely to have occurred
independently (FAO 2007).
Clearly, inferences about the location of origin from a single type of pattern of
molecular data (e.g. diversity levels) should only be made with caution because they can
be unsatisfactory or even potentially misleading. For example, levels of molecular
diversity in domestic breeds are expected to be highest near the centre of origin, assuming
that dispersal away from the centre would lead to loss of genetic variation due to repeated
founder effects (Loftus et a1. 1999). This pattern is indeed seen in cattle (Troy et al. 2001)
and sheep (Townsend 2000), but in goats, mtDNA variation is apparently not higher in the
Fertile Crescent region compared to most other continental regions. For example, the
mtDNA diversity (mean number of base changes between two sequences) within the Near
East, Europe, and Asia is approximately equal (10 bp differences). Rather, it is advisable
to incorporate information from several analyses, such as the geographic distribution of
haplogroups and also historical or temporal distributions, e.g. using ancient DNA, and
archaeological data (Luikart et al. 2001; Luikart et al. 2006).
However there are still uncertainties about the existence of some domestication
centres for some species, the following geographic areas are important primary centres of
origin and, therefore, diversity of livestock species: the Andean chain of South America
(llamas, alpacas, guinea pigs); central America (turkeys, Muscovy ducks); northeast Africa
(cattle, donkeys); southwest Asia including the Fertile Crescent (cattle, sheep, goats, pigs);
the Indus valley region (cattle, goats, chickens, riverine buffaloes); Southeast Asia

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Chapter 2 Introduction

(chickens, Bali cattle); east China (pigs, chicken, swamp buffaloes); the Himalayan
plateau (yaks); and north Asia (reindeer) (FAO 2007).

Figure 2.5. Major centres of livestock domestication, based on archaeological and

molecular genetic information.

It is important to remember, however, that genetically independent domestication

events are not necessarily culturally, or even entirely biologically, independent.
Knowledge of domestication can move between peoples and be applied to local wild plant
and animal resources. It is also possible that many of the apparently independent
domestication events in animals arose when either domestic males or females (or perhaps
both) were moved into an area and served as a kind of seed stock, breeding with local wild
populations. Depending on the sex of the domestic seed stock and the lineage traced by
genetic markers (maternal or paternal), this level of contact could well go undetected.
Ancient livestock DNA studies and osteometric information from archaeological sites are
important tools to address these issues (Zeder 2006).

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Chapter 2 Introduction

3.4. Complex patterns of genetic structure of domesticates

The use of genetic markers has revealed an extraordinary amount of variation and
complexity in the domestication of livestock, in terms of the numbers and types of
progenitors that contributed genetic material during domestication, and the number of
occasions that similar stocks were domesticated. So, what do these complex patterns of
past domestication imply for modern patterns of genetic diversity across individuals,
breeds, domestic ‘species’ and geographical zones? (Bruford et al. 2003)

Table 2.2. Summary of genetic and archaeological information for different domestic
species (FAO 2007).

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Chapter 2 Introduction

3.5. Goat Domestication

Goats were among the first farm animals domesticated, 10,500 years ago,
contributing to the rise of the ‘‘Neolithic revolution’’. Goat domestication was an integral
part of the rise of agriculture and the adoption of agricultural practices throughout much of
the world. Insights into the evolution and spread of goats are likely to deepen our
understanding of the origin and spread of agriculture and the rise of early human
civilizations. Archaeological and morphological studies suggested that the domestic goat

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Chapter 2 Introduction

(Capra hircus) was domesticated from the bezoar (Capra aegagrus) in the Fertile
Crescent (Meadow 1996; Porter 1996; Pringle 1998; Zeder & Hesse 2000; Zeder 2005;
Zeder 2006c). This origin was confirmed by genetic studies based on mitochondrial
(Manceau et al. 1999a; Mannen et al. 2001; Takada et al. 1997) and nuclear DNA
(Pidancier et al.2006; Luikart et al. 2006). The first archaeological evidence traces back as
far as ca. 10,500 cal. B.P. in the high Euphrates and Tigris valleys, in Southeastern
Anatolia (Peters et al.1999; Peters et al. 2005) and 9,900-9,500 cal. B.P. in the Zagros
mountains (Zeder & Hesse 2000; Zeder 2005).
People began to domesticate wild goats in highland area of Ganj Dareh in the Zagros
Mountains of western Iran. Metrical analyses of patterns of sexual dimorphism in modern
bezoars (Capra aegagrus) skeletons using direct accelerator mass spectrometry
radiocarbon dates allow sex-specific age curves to be computed for archaeofaunal
assemblages. A distinct shift to selective harvesting of sub-adult males marks initial
human management and the transition from hunting to herding of the species. In fact, early
herders mainly killed young males for meat and kept most females and a few older males
as breeding stock. In contrast, hunters interested in a quicker return on their effort often
targeted the largest males in a herd or killed many animals at once. Goats in these early-
managed herds probably looked much like wild goats, both physically and genetically. As
much as 500 years later, managed herds and their herders expanded out of this highland
homeland of initial domestication and into adjacent, less-optimal areas like Dehluran
Plain, where Ali Kosh is situated. Moving into these lowland areas undoubtedly
represented a substantial departure from the environmental conditions that prevailed in
their native highland habitats. It also ended any potential for interbreeding between
managed and wild goats. The more conservative harvest profile at Ali Kosh, later
slaughter of both young males and older females may be a response to the loss of easy
access to wild animals for restocking. The genetic isolation from wild populations, plus
the impact of tighter human control of breeding, undoubtedly resulted in the changes in
horn morphology documented at Ali Kosh. These factors, coupled with more arid
environmental conditions and poorer pasture opportunities, also may have contributed to a
reduction in the size of these animals (Zeder 2006c). Over time, isolation of managed
herds and the introduction of selective breeding produced changes in domesticated goats.

After the initial plant and animal domestications in the Near East, ca. 11,500 and
10,500, respectively, years ago (Harris 1996; Cauvin 2000), Neolithic culture diffused into

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Chapter 2 Introduction

Europe along two main routes (Diamond & Bellwood 2003). From their initial
domestication areas, goats also were introduced into Europe by following these routes.
Archaeological data and radiocarbon dates on seeds or bones provide support for an earlier
arrival in Western Europe (namely France) via the ‘‘Mediterranean’’ route rather than the
‘‘Danubian’’ route (Figure 2.6).

Figure 2.6. Map of goats introduction routes from their initial domestication areas into
Europe along ‘‘Mediterranean’’ and ‘‘Danubian’’ route (From Guilaine 2003; Fernández
et al. 2006).

Map of Figure 2.6 shows occidental part of the current geographic distribution of the
wild goat, Capra aegagrus (dotted area), as well as the two main waves for the initial
advancement of the Neolithic culture into Europe: the Mediterranean route and the
Danubian route. The location of Baume d’Oullen (an archaeological site in France) is
indicated by a star. The dates on the map are calibrated radiocarbon date-derived B.P. (cal.
B.P.). Solid-line arrows indicate main flow; broken-line arrows indicate possible
secondary flows. Dark gray zones indicate the area of the Impressa culture (8,000–7,500
cal. B.P.); light gray zones indicate the area of the Cardial and cultures (between 7,500 and
6,800 cal. B.P.) (Fernández et al. 2006).
This diffusion has been verified by archaeozoological analyses at Baume d’Oullen
and at a range of Early Neolithic sites from Southern Europe. In these sites, the number of
goats was low compare with sheep and even to cattle. These data indicate that Early

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Chapter 2 Introduction

Neolithic farmers were breeding and transporting relatively small flocks of goats. These
small local flocks were, however, probably more or less interbred at the regional scale
with other Early Neolithic flocks, because the contacts between the small human
communities were strong enough to generate large and rather homogeneous culture.
Therefore, the presence of high genetic diversity of such small goat populations in
southern France can be explained by extensive gene flow during the Neolithic expansion
between the Eastern and the Western Mediterranean Basin. Therefore, such an early
diversity seems likely to be explained by a diverse founding pool and a large effective
population size (i.e. global Ne) (Fernández et al. 2006).

4. Livestock transformations following domestication and consequences

on genetic diversity

The domestication process resulted in many changes in animals. Human favoured

several morphological changes. Domestic animals are generally smaller than their wild
ancestors. Smaller animals are easier to manage and to handle. They may also reach
puberty sooner, and large flocks or herds can be kept more easily (Hall 2004). In some
cases, human selection has deliberately resulted in extreme size differences, illustrated by
the small size of the Shetland pony and the large size of the Shire horse (Clutton-Brock
1999). These body size and form transformations from the wild ancestors were realized to
satisfy the demand for meat products (e.g. European beef breeds), or to cope with new
environmental pressures (e.g. Sahelian goats). Selection for muscular mass has often
resulted in greater muscular development of the hind quarters relative to the shoulders
(Hall 2004). An extreme example of selection for muscular mass is the double muscling
trait observed in some European beef breeds, and in some sheep and pigs breeds. In cattle,
the trait results from mutation at a single gene – the myostatin gene (Grobet et al. 1998).
In sheep it involves the callipyge gene (Cockett et al. 2005).
Fat pattern deposition may also show changes following domestication. For example,
reduced predation has encouraged fat deposition in domestic poultry. In domesticated
mammals, the hump of the Zebu and the tails of fat-tailed and fat-rumped sheep are
striking examples of selection for fat deposition. This exaggerated fat deposition may be
quite ancient, with fat-tailed sheep already common in western Asia by 3000 BC, and

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Chapter 2 Introduction

humped cattle depicted on cylinder seals from the ancient civilizations of Mohenjo-Daro
and Harappa in the Indus Valley about 2500 to 1500 BC (Clutton-Brock 1999).
Great variation is found in the wool and hair coats of most domestic species. For
example, sheep breeds of alpine regions have particularly thick woolly coats, while breeds
from the African Sahel lack wool. These changes were probably the result of mutations
followed by artificial selection, perhaps as early as 6000 BC, as illustrated by a statuette of
a woolly sheep found in Iran (Clutton-Brock 1999).
Coat and plumage colorations were also selected by the environment, with light
coloured animals being more adapted to hotter environments and dark coloured animals to
cooler environments (Hall 2004). Coat colours have also been influenced by cultural
selection. Livestock breeders in the developed world often favour uniformity in coat
colour, but in the tropics diversity in coat colour may be preferred for ceremonial reasons,
or simply to facilitate the identification of individual animals (Poland et al. 2003).
Understanding the origin and the subsequent history and evolution of domestic
animals is essential to the design of sustainable conservation and utilization strategies of
the genetic resources. Livestock diversity originates from the wild ancestors, and was
subsequently shaped through the processes of mutation, genetic drift, and natural and
human selection. Only a subset of the diversity present in the ancestral species survived, in
the domestic counterparts. However, domestic livestock diversity has been continuously
evolving. Reshuffling of genes at each generation, mutation, and cross-breeding or
admixture of different gene pools has offered new opportunities for natural and human
selection. This has been the basis of the enormous gains in productivity achieved in
commercial breeds, and of the adaptation of indigenous livestock to highly diverse and
challenging environments. However, the world’s livestock diversity is currently shrinking,
with rapid and uncontrolled loss of unique and often uncharacterized animal genetic
resources. If a breed or population becomes extinct, this means the loss of its unique
adaptive attributes, which are often under the control of many interacting genes, and are
the results of complex interactions between the genotype and the environment.

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Chapter 2 Introduction

5. Conservation Genetics and implications for conservation

Molecular genetic studies results can be utilized for scientific management and
conservation of wild animals and their domestic descendents. In the past, the
domestication of plants and animals was a key step in human evolution, allowing the
development of our current societies. We can anticipate that domestic plants and animals
will continue to play a key role in the future, but many plant varieties and animal breeds
are endangered (Esquinas-Alcazar 2005; Taberlet et al. 2007). Genetic data should help to
promote a sustainable use of the genetic resources. Sound conservation strategies must
rely on the knowledge of the levels of genetic diversity within and between breeds, the
knowledge of the adaptive geographic variation, the inventories of potential genetic
resources including the wild ancestor, and the assessment of colonisation routes out of the
domestication centres. Particular attention should be paid to wild ancestors, and to
traditional breeds located close to the domestication centres. Finally, as for wild animals, it
might be useful to consider the concept of evolutionary significant units (ESUs) (Ryder
1986; Moritz 1994) and to also apply it to domestic species. According to the current loss
of genetic diversity in domestic breed at the worldwide level (FAO 2007), it is extremely
important to design in the short term sound strategies for preserving the evolutionary
potential of domestic animals and achieving sustainable animal farming.

Figure 2.7. The habitat of Capra aegagrus in Dena Protected Area in Iran (Photo by S. Naderi)

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Chapter 3. mtDNA diversity of goats
Chapter 3 mtDNA diversity of goats

Chapter 3. Large-scale mitochondrial DNA analysis of the domestic goat

reveals six haplogroups with high diversity

Research Article

Saeid Naderi1,2, Hamid-Reza Rezaei1,3, Pierre Taberlet1, Stéphanie Zundel1, Seyed-Abbas

Rafat4, Hamid-Reza Naghash1, Mohamed A. A. El-Barody5, Okan Ertugrul6, François
Pompanon1 and the Econogene Consortium7

PLoS ONE 2(10): e1012. doi:10.1371/[Link].0001012

1 Laboratoire d'Ecologie Alpine, CNRS-UMR 5553, Université Joseph Fourier, BP 53,

38041 Grenoble Cedex 09, France.
2 Natural Resources Faculty of Guilan University, Guilan, Iran.
3 Environmental Sciences Department, Gorgan University of Agriculture and Natural
Resources, Gorgan, Iran.
4 Animal Science Department, Faculty of Agriculture, University of Tabriz, 51664,
Tabriz, Iran
5 Animal Production Department, Faculty of Agriculture Minia University, Minia, Egypt
6 Department of Genetics, Faculty of Veterinary Medicine, Ankara University, 06110
Dışkapı Ankara, Turkey
7 [Link]

Institution at which research was done: Laboratoire d’Ecologie Alpine, Université

Joseph Fourier, Grenoble, France.
Corresponding author: François Pompanon, Laboratoire d'Ecologie Alpine,
CNRS-UMR 5553, Université Joseph Fourier, BP 53, 38041 Grenoble Cedex 09, France
Tel: +33(0)4 76 51 42 78; Fax: +33(0)4 76 51 42 79
E-mail: franç[Link]@[Link]
Key words: Domestic goat, Mitochondrial DNA (HVI), haplogroup, Genetic structure,
phylogeny, Capra hircus

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Chapter 3 mtDNA diversity of goats

Abstract

Background. From the beginning of domestication, the transportation of domestic

animals resulted in genetic and demographic processes that explain their present
distribution and genetic structure. Thus studying the present genetic diversity helps to
better understand the history of domestic species. Methodology/Principal Findings. The
genetic diversity of domestic goats has been characterized with 2430 individuals from all
over the old world, including 946 new individuals from regions poorly studied until now
(mainly the Fertile Crescent). These individuals represented 1540 haplotypes for the HVI
segment of the mitochondrial DNA (mtDNA) control region. This large-scale study
allowed the establishment of a clear nomenclature of the goat maternal haplogroups. Only
five of the six previously defined groups of haplotypes were divergent enough to be
considered as different haplogroups. Moreover a new mitochondrial group has been
localized around the Fertile Crescent. All groups showed very high haplotype diversity.
Most of this diversity was distributed among groups and within geographic regions. The
weak geographic structure may result from the worldwide distribution of the dominant A
haplogroup (more than 90% of the individuals). The large-scale distribution of other
haplogroups (except one), may be related to human migration. The recent fragmentation of
local goat populations into discrete breeds is not detectable with mitochondrial markers.
The estimation of demographic parameters from mismatch analyses showed that all groups
had a recent demographic expansion corresponding roughly to the period when
domestication took place. But even with a large data set it remains difficult to give relative
dates of expansion for different haplogroups because of large confidence intervals.
Conclusions/Significance. We propose standard criteria for the definition of the different
haplogroups based on the result of mismatch analysis and on the use of sequences of
reference. Such a method could be also applied for clarifying the nomenclature of
mitochondrial haplogroups in other domestic species.

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Chapter 3 mtDNA diversity of goats

Introduction

More than 10,000 years ago, the transition of humans from hunting to the
manipulation of the behavior of certain animals lead to the process of domestication [1].
This process contributed to the rise of human civilization by enabling people to settle into
a sedentary lifestyle. The goat was one of the first domesticated animals [2-4]. It was a
source of milk, meat, dung for fuel and materials for clothing and building such as hair,
bone and skin [1,5]. Archaeological studies suggested that the domestic goat Capra hircus
was domesticated from the bezoar Capra aegagrus in the Fertile Crescent [e.g. 6-8]. This
origin was confirmed by genetic studies based on mitochondrial [e.g. 9,10] and nuclear
DNA [11].
From the beginning of the domestication process, the exchange and transportation of
domestic animals has been related to human migration and trade. This resulted in genetic
(e.g., selection, gene flow) and demographic processes that explain the present worldwide
distribution of more than 300 different breeds of Capra hircus and their genetic structure
[2]. Thus, the present genetic diversity bears the molecular signature of past events, such
as rapid demographic expansions. Therefore, the study of this diversity helps to
reconstitute the evolutionary history of the goat [12] and could bring new facts that help to
understand the history of domestication.
Mitochondrial DNA is commonly used for the study of domesticated species. The
control region has been especially used for describing the genetic polymorphism of goats
[13], because it is variable and structured enough across the geographical range of the
species, and evolves at a constant rate [12]. Moreover, it allows maternal lineages to be
followed and is less sensitive to introgression from wild species than nuclear DNA [13].
However, studies on nuclear genes are needed because they give information on gene flow
and selection processes that had a great influence on the evolution of livestock species
[12].
Luikart et al. [13] conducted the first study of the overall genetic structure of
domestic goats at the worldwide scale. They analyzed 406 individuals representing 88
breeds from the old world. They found three mitochondrial haplogroups (A, B and C) that
diverged more than 200,000 years ago and have undergone demographic expansion at
different times. This would suggest multiple maternal origins of domestic goats or
introgression of other haplotypes after the first domestication event. Moreover, they

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Chapter 3 mtDNA diversity of goats

showed that most of genetic diversity occurred within breeds, and interpreted the very
weak geographic structure as the result of the extensive transportation of goats among
continents.
The initial global survey by Luikart et al. [13] has been followed by regional studies
describing more precisely the genetic diversity of goat breeds. However, these studies
were always realized in restricted geographic regions corresponding to different countries
such as Pakistan [14], India [15], China [16], South Korea [17], Sicily [18], Spain [19,20]
and Portugal [21]. The existence of three new haplogroups has been suggested [14,15,18].
However, this has sometimes been based only on a few individuals, and without
comparing the new divergent haplotypes to a sample representative of the worldwide
haplotype diversity. In general, the identification of a new haplogroup might be
controversial in the absence of standardized criteria. All previous studies describing the
mitochondrial polymorphism of domestic animals use the term of "maternal lineage" for
characterizing a group of closely related haplotypes. However, this term is ambiguous as it
usually corresponds to many haplotypes, and thus to many maternal lineages sensu stricto.
As a consequence, we propose to use "mitochondrial haplogroup" instead of "maternal
lineage", a term that is already in common use in genetic studies.
In this context, the goals of the present study are (i) to characterize the domestic goat
mtDNA diversity based on a worldwide sampling and make a global synthesis including
previous studies, (ii) to establish the relationships between mitochondrial haplogroups and
to propose a clear nomenclature, and (iii) to give standard criteria for the definition of
mitochondrial haplogroups. For this purpose we used data from previous studies (1484
sequences retrieved from GeneBank), and we analyzed 946 new samples from all over the
old world. New samples were especially taken from localities that have not been
adequately sampled before, and that may have played an important role in the history of
goat domestication (i.e., Middle East and especially the Fertile Crescent).

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Chapter 3 mtDNA diversity of goats

Results

Sequence polymorphism

The HVI fragment of the control region shows a high polymorphism with 336
variable sites over the 558 bp of the alignment. We observed 285 substitutions (226
transitions and 59 transversions) and 110 insertions/deletions (from 1 to 76 bp). The 2430
individuals correspond to 1540 different haplotypes.

Phylogenetic analysis and genetic structure of domestic goats

The Neighbor-joining tree of the 2430 domestic goats (Figure 3.1) shows 6 highly
divergent groups corresponding to different mitochondrial haplogroups called A, B, C, D,
F (according to previous studies) and G. Each group has high haplotype diversity (Table
3.1), and has been defined by high bootstrap values (except a bootstrap of 53 % for A;
Figure 3.1A), and by high mean pairwise distance with all other groups (see below). The
A haplogroup is the most represented when considering either the number of individuals
or the number of haplotypes and is highly dominant all over the old world (Table 3.1 and
Figure 3.2). Except for two individuals situated at the base of the B group, this clade is
composed of two sub-groups, B1 (35 haplotypes) and B2 (9 haplotypes), as previously
defined by Chen et al. [16]. The B group is mostly found in whole Asia, with a few
individuals from the Sub-Saharan Africa and one European goat from Greece. The B2
individuals are restricted to China and Mongolia. Goats from the C group are from whole
Asia and Europe and the D group is present in the whole Asia and Northern Europe. The
three goats from the F group are from Sicily. The G group has not been reported until now,
and is present in Middle East and Northern Africa, near the Fertile Crescent.

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Chapter 3 mtDNA diversity of goats

Figure 3.1. Neighbor-joining trees of domestic goat based on 1540 mtDNA haplotypes (A)
and on the 22 reference mtDNA haplotypes (B). Distances were calculated using the
Kimura 2-Parameter model with gamma correction (alpha = 0.28). On the (A) tree, the
numbers on the branches represent bootstrap values out of 1000 replications, and the stars
point out the position of reference individuals for each haplogroup used to construct the
(B) tree (see Table 3.5).

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Chapter 3 mtDNA diversity of goats

Table 3.1. Genetic diversity of goat mtDNA haplogroups

haplogroup # individuals (%) # haplotypes (%) haplotype diversity

A 2208 (90.86) 1440 (93.51) 0.9992 ± 0.0001

B 144 (5.92) 46 (2.99) 0.9000 ± 0.0197

B1 107 (4.40) 35 (2.27) 0.8402 ± 0.0333

B2 35 (1.44) 9 (0.58) 0.8151 ± 0.0481

C 35 (1.44) 23 (1.49) 0.9714 ± 0.0136

D 13 (0.54) 10 (0.65) 0.9487 ± 0.0506

F 3 (0.12) 3 (0.19) 1.0000

G 27 (1.11) 18 (1.17) 0.9544 ± 0.0254

The haplotype diversity is very high all over the Eurasia and Africa with a value
above 0.97 in 39 of the 54 studied countries (Table 3.2). More than 77% of the mtDNA
variation is distributed within breeds while about 11% is found among breeds within
geographic regions and 12 % among geographic regions (Table 3.3). Nevertheless this low
but significant geographic structure is coherent with the fact that all breeds are composed
of individuals from the A group, with eventually a lower percentage of individuals from
other haplogroups (for about 25% of the breeds). This low geographic structure is also
confirmed by the distribution of all haplogroups that are present in several regions (except
for F). Most of the mtDNA diversity is distributed among groups and within geographic
regions, while less than 4% of this variability is found among regions within groups (Table
3.3).

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Chapter 3 mtDNA diversity of goats

Figure 3.2. Geographic distribution of domestic goat mtDNA haplogroups. The size of
each circle is proportional to the sample size and each specific haplotype is represented by
a different colour.

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Chapter 3 mtDNA diversity of goats

Table 3.2. Geographic origin and characteristics of the studied domestic goat

# of # of # of # ind /
region country Haplotype diversity Accession numbers
breeds individuals haplotypes haplogroup

Bhutan 1 5 5 A:5 1.0000+/-0.1265 AJ317851-55 (Luikart et al. 2001)

AJ317569-70 (Luikart et al. 2001);
DQ089106-13; DQ089116;
DQ089135; DQ089147;
DQ089155-9; DQ089186-8;
DQ089191-209; DQ089212-16;
DQ089218-19; DQ089221-2;
A:275;
DQ089237-47; DQ089249-54;
B1: 63;
China 13+U 382 154 0.9827+/-0.0027 DQ089256-57; DQ089269-70;
B2: 34; C:7;
DQ089272-80; DQ089282-304 ;
D: 3
DQ089350 (Chen et al. 2005);
AY853278-301 (Zhang et al.
2004); DQ121491-588;
DQ121590-618 (Liu et al. 2006);
Eastern DQ188849-903 (Liu et al. 2005);
Asia (EA) AY860871-942 (Zhang et al. 2004)
AB044295- 304 (Mannen et al.
Laos 1 10 7 A:4; B1: 6 0.9778+/-0.0540
2001)
AJ317553; AJ317831-32;
Malaysia 1 16 6 A:2; B1:14 0.8583+/-0.0626 AJ317828-29 (Luikart et al. 2001);
EF618221- 31
AJ317534 -38; AJ317545-52;
A:19; B2:1;
Mongolia 2+U 21 21 1.0000+/-0.0147 AJ317833-34 (Luikart et al. 2001);
C:1
EF618234- 39
South Korea U 6 4 A:6 1.0000+/-0.0962 DQ217780- 85 (Lee et al. 2005)

AJ317566-68 (Luikart et al. 2001);

Vietnam 1 4 3 A:4 0.8333+/-0.2224
EF618541

A:207 ;
Iran 3+U 222 161 0.9970+/-0.0008 EF617863- EF618084
G:15
Iraq 1 7 6 A:7 1.0000+/-0.0764 AJ317762-68 (Luikart et al. 2001)
AJ317769-73 (Luikart et al. 2001);
Jordan 2 19 16 A:19 0.9825+/-0.0223
EF618191- 204
AJ317533; AJ317539;AJ317554-
55; AJ317557-59; AJ317563-65;
A:56; AJ317826; AJ317845-50;
Middle Pakistan 18 73 55 B1:12; 0.9855+/-0.0076 AJ317861-63 (Luikart et al. 2001);
East (ME) C: 2 ; D: 3 AB110552-589(Sultana et al.
2003);
EF618253- 63
AJ317752-59 (Luikart et al. 2001);
Saudi Arabia 3 45 39 A:40; G: 5 0.9949+/-0.0058
EF618309- 45
Syria 1 2 2 A:2 1.0000+/-0.5000 AJ317760-61 (Luikart et al. 2001)
AJ317736-751; AJ317842-43
Turkey 5 66 56 A:61; G: 5 0.9953+/-0.0038 (Luikart et al. 2001); EF618492-
539
Azerbaijan 1 5 5 A:4 ; B1:1 1.0000+/-0.1265 EF617702- 6
Dagestan 1 2 2 A:2 1.0000+/-0.5000 EF617708- 9
AJ317827; AJ317856-57;
AJ317540-41; AJ317830;
Western A:373 ;
AJ317542-44; AJ317560-62;
Asia (WA) India 5+U 387 207 B1:7; 0.9937+/-0.0008
AJ317571-72 (Luikart et al. 2001);
C:4; D:3
AY155674-AY156039 (Joshi et al.
2004); EF617856 - 62
Kazakhstan 1 7 7 A:7 1.0000+/-0.0764 EF618205- 11
Kyrgyzstan 1 8 7 A:5 ; D: 3 0.9643+/-0.0772 EF618212- 19
Northern Algeria 1 3 3 A:3 1.0000+/-0.2722 AJ317777-79 (Luikart et al. 2001)
Africa AJ317780-83; AJ317795-801
(NAF) Egypt 3 29 24 A:27 ; G: 2 0.9901+/-0.0116 (Luikart et al. 2001); EF617711-
28

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Chapter 3 mtDNA diversity of goats

Libya U 1 1 A:1 1.0000+/-0.0000 EF618220

AJ317784 -88 (Luikart et al. 2001);
Morocco 1 6 5 A:6 0.9333+/-0.1217
EF618233
AJ317810-811; AJ317823-25
3
Nigeria 12 12 A:12 1.0000+/-0.0340 (Luikart et al. 2001); EF618246-
52
Senegal 1 3 3 A:3 1.0000+/-0.2722 AJ317816-18 (Luikart et al. 2001)
Tunisia 1+U 6 5 A:6 1.0000+/-0.0962 AJ317789-794 (Luikart et al. 2001)
AJ317804-809 (Luikart et al.
Mozambique 1 8 5 A:8 0.9286+/-0.0844
2001); EF618240- 1
Sub-
Namibia 2 4 1 A:2; B1: 2 0.8333+/-0.2224 EF618242- 5
Saharan
Africa AJ317812-15; AJ317819-20;
(SAF) South Africa 3+U 15 11 A:12; B1: 3 0.9429+/-0.0542 AJ317844; AJ317821-22 (Luikart
et al. 2001); EF618351- 56
AJ317802-803 (Luikart et al.
Zimbabwe 1 4 2 A:4 0.8333+/-0.2224
2001); EF618545- 6
Austria 2 24 18 A:23; D:1 0.9783+/-0.0187 EF617678- 701
AJ317650 (Luikart et al. 2001) ;
Denmark 1 2 1 A:2 1.0000+/-0.5000
EF617710
AJ317592; AJ317841 (Luikart et
England 1 3 2 A:3 0.6667+/-0.3143
al. 2001); EF617729
AJ317575-83; AJ317713-19;
AJ317723-25; AJ317629-30
France 7 79 61 A:77 ; C: 2 0.9932+/-0.0039
(Luikart et al. 2001); EF617730-
87
AJ317586; AJ317627-28
Germany 5 32 25 A:32 0.9919+/-0.0099 ; AJ317649 (Luikart et al. 2001);
EF617788- 815
AJ317587 (Luikart et al. 2001);
Iceland 6 6 1 A:6 0.0000+/-0.0000
EF617851- 55
AJ317588-91 (Luikart et al. 2001);
Ireland 1 6 4 A:6 0.8667+/-0.1291
EF618085- 6
Northern Norway 1 3 3 A:3 1.0000+/-0.2722 AJ317593-95 (Luikart et al. 2001)
Europe AJ317584-85; AJ317651-52
(NE) Poland 4 27 22 A:27 0.9943+/-0.0119 (Luikart et al. 2001); EF618264-
86
Slovakia 1 2 2 A:2 1.0000+/-0.5000 AJ317653-54 (Luikart et al. 2001)
AJ317731; AJ317835; AJ317837
Slovenia 1 8 3 A:2; C: 6 0.7143+/-0.1227 (Luikart et al. 2001); EF618346-
50
AJ317637 (Luikart et al. 2001);
Sweden 1 9 7 A:9 0.9722+/-0.0640
EF618415- 22
AJ317573-74; AJ317596-99;
AJ317605; AJ317619-24;
AJ317626; AJ317631-36;
Switzerland 11 104 74 A:94; C:10 0.9925+/-0.0026
AJ317836; AJ317838- 40;
AJ317638-48 (Luikart et al. 2001);
EF618423- 91
AJ317600-604 (Luikart et al.
Ukraine 1 6 4 A:6 0.9333+/-0.1217
2001); EF618540
AJ317655-58 (Luikart et al. 2001);
Wales 7 7 4 A:7 0.8095+/-0.1298
EF618542 - 44
Southern Albania 6 77 65 A:77 0.9969+/-0.0028 EF617601- 77
Europe
(SE) AJ317774-76 (Luikart et al. 2001);
Cyprus 1 4 3 A:4 0.8333+/-0.2224
EF617707
AJ317686-97 (Luikart et al. 2001);
Greece 2+U 47 39 A:46 ; B1:1 0.9935+/-0.0061
EF617816- 50
AJ317674-78; AJ317680-85
Italy 11 115 95 A:115 0.9969+/-0.0018 (Luikart et al. 2001); EF618087-
190
AJ317659-AJ317702-AJ317708
Malta 2 4 4 A:4 1.0000+/-0.1768
(Luikart et al. 2001); EF618232

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Chapter 3 mtDNA diversity of goats

AJ317660-69; AJ317698-701;
AJ317720-22; AJ317726-30;
Portugal 8 321 164 A:320 ; C:1 0.9941+/-0.0009 AJ317732-35 (Luikart et al. 2001);
AY961629-697; AY961700- 916
(Pereira et al_2005); EF618287- 95

AJ317606-618 (Luikart et al.

Romania 6 26 23 A:26 0.9908+/-0.0133
2001); EF618296- 308
Sicily 1 67 22 A:64; F: 3 0.9701+/-0.0073 DQ241305-71 (Sardina et al. 2006)
AJ317625; AJ317670-73;
AJ317679; AJ317703-
Spain 9+U 73 59 A:71;C:2 0.9962+/-0.0032 4;AJ317705-7; AJ317709-12
(Luikart et al. 2001);EF618357-
414

Note: U: Individuals from undefined breed(s)

Table 3.3. Partition of the genetic variance among haplogroups, breeds and continental
regions revealed by hierarchical AMOVAs

AMOVA haplogroups / regions AMOVA regions / breeds

Among Among
Source of Among regions Within Among breeds Within
variation haplogroups within regions regions within breeds
haplogroups regions
d.f. 5 20 2404 6 166 1429
% of
74.62 3.56 21.82 12.06 10.79 77.14
variation
P value <0.0001 <0.0001 <0.0001 <0.0001

Demography of mitochondrial haplogroups

Because of the low number of goats in the F group, demographic parameters were
not estimated for this group. The overall mismatch distribution shows a multi-modal
distribution (Figure 3.3). The first peak with a maximum of 10 pairwise differences
corresponds to the differences between haplotypes from the same group. Two other peaks
with maxima at 27 and 39 pairwise differences correspond to differences between
haplotypes from different groups. The distributions of within-groups and between-groups
pairwise differences have a very thin overlap around 20 mismatches. The mismatch
distribution analysis reveals a unimodal bell-shaped distribution of pairwise sequence
differences for all haplogroups (Figure 3.3), except for B that is bimodal (data not shown).
B1 and B2 are unimodal, and individuals from these sub- groups generally differ by 8 or 9
mismatches (always less than 14 mismatches). This unimodal pattern that is less clear for

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Chapter 3 mtDNA diversity of goats

the D group, perhaps because of the low sample size (n=13), would be coherent with
recent demographic expansions. The time of expansion would differ according to the
group, as suggested by the different means of pairwise distribution (Figure 3.3) and the
estimations made under a model of pure demographic expansion [22] (Table 3.4).
However, the validity of the expansion model used for estimating the expansion time is
only accepted for the A, C groups (SSD P-Values <0.00001 and ≤ 0.05 respectively see
Table 3.4). All groups have high growth rates indicating high demographic expansion
(Table 3.4). The estimates differ according to the groups, but the overlapping of
confidence intervals, as well as the different sample sizes, preclude further interpretation.

Figure 3.3. Mismatch distributions for mtDNA haplogroups of domestic goats. For the
overall dataset, the distribution of pairwise differences were realized separately for
comparisons between and within haplogroups.

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Chapter 3 mtDNA diversity of goats

Table 3.4. Estimation of demographic parameters from genetic data

Validity of the expansion Rough estimation

τ Growth rate
haplogroups model of Expansion
(0.95 CI) (0.95 CI)
SSD (P-value) time
A 10.07 (9.74-10.42) 0.00071 (P <0.0001) ~ 9000 - 9700 308 (199-344)
B1 1.855 (0.73-3.19) 0.0008 (P =0.70) - 333 (201-412)
B2 1.584 (1.10-2.65) 0.0095 (P =0.20) - 108 (14-324)
C 6.37 (4.99-7.84) 0.00795 (P =0.05) ~ 4600 - 7300 185 (158-291)
D 9.10 (5.50-13.01) 0.0141 (P =0.20) - 334 (173-509)
G 5.79 (2.85-11.22) 0.0021 (P =1.00) - 209 (144-293)

Note. - See material and methods for the methods used for estimating the demographic
parameters. CI: Confidence Interval. SSD: sum of square deviations between the observed
and the expected mismatch distributions.

Discussion

High mtDNA diversity in domestic goat

The very high mt DNA diversity may partly result from a high mutation rate of the
control region. Higher pedigree divergence rates than phylogenetic divergence rates have
been shown for the control region in human [23] and other animals (e.g.,[24, 25]). This
could explain that we observe a higher diversity than the one expected with the
phylogenetic mutation rate estimated for Bovidae (i.e., 30.1 % of divergence per Myr on
the total control region sequence based on the Bos/Bison divergence [26]). Such high
variability could also result from the selection of polymorphism but, to our knowledge,
this has never been shown for the control region. Another explanation would be the
capture of a large part of the diversity of the wild ancestor (i.e., the bezoar) during the
domestication, with a large maternal effective population size. Testing this last hypothesis
requires comparing the diversity of goats to that of the bezoar [27].

Characteristics and nomenclature of mitochondrial haplogroups

Five reliable mitochondrial haplogroups have previously been described in domestic

goats [13-15,18]. However, most of the previous studies were based on local samples and

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Chapter 3 mtDNA diversity of goats

thus only considered a part of the whole haplotype variability. Therefore, it may be
difficult to assess the pertinence of defining a new group on the base of few haplotypes. It
would also be difficult to make the correspondence between several studies analyzing
samples from different geographic origins. Our study can lead to a clear nomenclature of
goat mitochondrial haplogroups, because we analyzed 2430 goats representing 1540
different haplotypes from all over Africa, Asia and Europe (946 new sequences mainly
from the region of domestication and 1484 sequences from previous studies). We revealed
the existence of 6 highly divergent groups. Five of them (A, B, C, D and F) have already
been described, and one (G) is a new group. The two sequences that have been previously
used to define the E group [15] now fall within the A haplogroup. This is partly due to the
finding of new haplotypes, which are intermediate between those from A and E used by
Joshi et al. [15]. Therefore, the E group cannot be considered as a mitochondrial
haplogroup anymore. The B clade is composed of two groups (B1 and B2) that have
previously been described as "sub-lineages" by Chen et al. [16]. We agree that the B1 and
B2 are part of the same haplogroup because the genetic divergence between them
(pairwise differences always lower than 14 mismatches) is lower than the divergence
between all pairs of haplogroups (more than 20 mismatches). They must be considered as
two subgroups because even with a low divergence they are supported by robust bootstrap
values.

Standard criteria for defining goat mitochondrial haplogroups

More generally, previous considerations point out the problem of defining groups
and sub-groups. A new haplogroup is defined when it highly diverges from all other
haplotypes. However, the haplogroups may change over time, as more and more
haplotypes will be available. We faced this situation for the E haplogroup that is no valid
any more. There is therefore a need for standard and easy-to-use criteria in order to assign
new goat haplotypes to existing haplogroups or to define new haplogroups. A haplotype
can be related to an existing group if it presents a moderate genetic divergence from this
group. The difficulty may be to define what is a “moderate” divergence. It can be deduced
from the distributions of pairwise sequence differences within and between haplogroups.
For goats, almost all haplotypes from the same group differ by less than 20 mismatches
(whatever the group) while haplotypes from different groups usually present more than 20

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Chapter 3 mtDNA diversity of goats

mismatches (Figure 3.3). This threshold value would give a quick and easy indication for
almost all studied haplotypes. However, it may be inadequate for some haplotypes (about
1% in our study) because the two mismatch distributions overlap.
Given the increasing number of sequences available, analyzing new haplotypes
together with all previously published sequences will be time consuming and will require
huge computational resources. Moreover several programs cannot be used because the
algorithm complexity does not allow managing such datasets. Especially when a few
haplotypes from restricted localities are studied, their assignation to haplogroups should be
quick and easy. For a first approach, an accurate solution would be to place the new
different haplotypes in a phylogenetic tree containing sequences of reference
representative of the diversity of C. hircus mitochondrial DNA. For this purpose we have
selected 22 haplotypes representing the variability of the 6 present goat mitochondrial
haplogroups (Table 3.5 and Figure 3.1B).

Table 3.5. The 22 reference individuals of the 6 domestic goat haplogroups

Geographic origin Accession

haplogroup Reference
(Country) Number
A India AY155721 Joshi et al. 2004
A Italy EF618134 This Study
A France EF617779 This Study
A Jordan EF618200 This Study
A Iran EF617945 This Study
A Iran EF617965 This Study
B1 Laos AB044303 Mannen et al. 2001
B1 Azerbaijan EF617706 This Study
B2 Mongolia AJ317833 Luikart et al. 2001
B2 China DQ121578 Liu et al. 2006
C India AY155708 Joshi et al. 2004
C Switzerland AJ317838 Luikart et al. 2001
C Spain EF618413 This Study
C China DQ188892 Liu et al. 2005
D India AY155952 Joshi et al. 2004
D Austria EF617701 This Study
D China DQ188893 Liu et al. 2005
F Sicily DQ241349 Sardina et al. 2006
F Sicily DQ241351 Sardina et al. 2006
G Iran EF618084 This Study
G Turkey EF618535 This Study
G Egypt EF617727 This Study

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Chapter 3 mtDNA diversity of goats

Four of the 1540 haplotypes present a tandemly repeated sequence of 76 bp. Three
individuals are from the A group (from Iran, Morocco and India) and one from the B1 sub-
group (Malaysia). Such tandem repeats are common in vertebrate species [28] and have
already been found in the Bovidae family [29]. They are attributed to slippage-mispairing
events that are more likely to appear in regions where the polymerase activity is
interrupted [28]. This phenomenon corresponding to a single duplication event is found in
a few individuals from different haplogroups, and has occurred more than once in the
history of goats.

Genetic structure of domestic goats

Our results show that most of the genetic variation is found among goat haplogroups,
with a weak phylogeographic structure. The strongly dominant A group (91 % of the
goats) is distributed worldwide, and even if the other groups have more restricted
distributions they still occupy large geographic areas (Figure 3.2). The F group is the
exception, with three haplotypes restricted to a single locality (Sicily) that could have been
brought along from recently captured wild goats. However, the sampling effort may still
be insufficient to see the whole distribution of haplogroups other than A, because of their
low frequency. The differences among geographic regions at the worldwide scale are low
(about 12%) but significant. This is concordant with previous results showing a very weak
phylogeographic structure of goats [13] and sheep [30,31] compared to cattle [32,33]. The
genetic differences among continental regions could partly result from the differential
geographic distribution of mitochondrial haplogroups. However, there is still a low but
significant genetic variation (3.5%) among region within groups, indicating regional
differentiations of haplotypes. At the regional scale, the lack of geographic structure has
also been reported in several places [16,19,21] while a structure has been found in India
[15]. The weak phylogeographic structure found today in goats has been explained by a
high mobility of this species in relation to human migration and commercial trade
[12,13,34]. This mobility would have been higher than those of cattle due to their
versatility in feeding habits and ability to live under extreme conditions [1]. However, the
mixing of goat haplogroups could have existed before the worldwide translocation of
goats. The presence of goats in Cyprus 10,000 years ago [35] suggests that goats could
have been translocated within the domestication area since the first domestication events.

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Chapter 3 mtDNA diversity of goats

Moreover, we cannot exclude that the mt-haplogroups were already mixed in the wild
ancestor before domestication. When considering the local scale, the genetic pattern of
domestic goats also seems related to human history. For instance, the geographic structure
found in Indian goats would have a common historical basis in the sequential migrations
of human populations with different cultural and linguistic characteristics [15].
However, the information given by mitochondrial markers is limited because it does
not detect male-mediated gene flow and does not predict the nuclear genomic diversity
[12]. In particular, the breeds cannot be distinguished on the base of mtDNA [16,19, 20]
while nuclear markers show a genetic structure [36-38]. Our study confirmed that more
than 77 % of the mtDNA variation is found within breeds and that nearly 25% of the
breeds are composed of at least 2 haplogroups. This is in accordance with the recent
fragmentation of local goat populations into discrete breeds about 200 years ago, under
strong selection pressures on a few phenotypic traits [39]. This structure can be seen on
nuclear markers linked to selected parts of the genome, but not on mitochondrial markers.
Then, looking at the evolutionary history of breeds using mtDNA markers could lead to
misinterpretation. For example, a breed composed of two mitochondrial haplogroups
would have a bimodal mismatch distribution due to within- and between-breeds pairwise
differences, and should not be interpreted in term of demographic history of the breed.
Thus, fully understanding the evolutionary history of domestic goats would also require
the use of nuclear markers.

Demography of mitochondrial haplogroups

The present structure of the genetic diversity retains the signature of past
demographic events and helps reconstitute the evolutionary history [40]. The estimation of
demographic parameters remains difficult because of the difficulties of verifying the
hypothesis of the models used, of estimating accurate initial parameters (e.g., absolute date
of domestication) and sometimes because of low sample sizes. However, rough
estimations from the present work and previous studies [13,15,16] are concordant and
agree on the same scenario. All haplogroups had a recent demographic expansion
corresponding roughly to the period when domestication took place about 10,000 years
ago. It is difficult to give relative dates of expansion because of large confidence intervals,
especially for D and G groups, but our results confirm that the expansions of B and C

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Chapter 3 mtDNA diversity of goats

groups were more recent than that of A [13]. Also, our results show that all groups had
high growth rates, with a tendency for slower growth in B2 sub-group and C and G. A
faster growth of A relative to C is in accordance with archaeozoological data: the
genotyping of fossil goats showed that about 7000 years ago A and C were equally
represented in Southern France [34] while A is strongly dominant in Southern Europe
now.

Limits of genetic data from domestic goats for reconstituting the history of
domestication

Divergence time between haplogroups has been estimated on adequate molecular

markers (mainly cytochrome b) between 103,000 and 597,800 years [13-16]. All these
values are far greater than the domestication time, showing that most of goat genetic
diversity existed before domestication, and that several haplogroups were domesticated in
one or several events. However, the genetic data available for domestic goats does not
permit furthering our understanding of the domestication process and identifying potential
domestication centre(s). A higher genetic diversity would have been expected near the
Fertile Crescent where the goat domestication took place according to archaeological data,
and where extensive sampling has been done. But the haplotype diversity is similar all
over the world (more than 80% of the countries with a haplotype diversity greater than
0.9), because of the high migration rates in domestic goats due to human migration and
commercial trade.
Moreover, the presence of a possible ancestral haplotype in a particular area does not
prove that this is a domestication centre, since many events could have occurred to mask
the real history (e.g., coalescence or founder effects). For instance the domestication of a
B sub-group in China supported by genetic data [16] is doubtful since the wild ancestor of
the domestic goat (i.e. the bezoar Capra aegagrus) has credibly never been present in this
area [11, 41]. Overall, in order to fully understand the domestication of goats it is
necessary to characterize the genetic diversity of wild goat species, and to establish the
evolutionary relationships between wild and domesticated haplotypes.

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Chapter 3 mtDNA diversity of goats

Materials and methods

Sampling and DNA extraction

Samples were collected from 946 individuals from 42 countries of the old world (See
Table 3.2) from which 569 individuals were studied within the Econogene project
([Link]). Samples consisted of ear tissue preserved in ethanol 95% until
extraction, or of blood collection. DNA was extracted from tissue using the Qiagen
DNeasy tissue kit following the manufacturer’s instructions, and from blood samples
using QIAamp DNA blood kit.
To have a good coverage of the goat breeds, the dataset was completed with 1484
sequences containing the Capra hircus HVI control region (450 to 1200 bp long) retrieved
from GenBank (Table 3.2).

DNA amplification and sequencing

The HVI segment of the control region was sequenced for all blood and tissue DNA
extracts. Using the primers CAP-F (5’-CGTGTATGCAAGTACATTAC-3’) and CAP-R
(5’-CTGATTAGTCATTAGTCCATC-3’), we amplified a fragment of 598 bp (without
primers) that corresponds to the positions 15,653 to 16,250 on the complete goat
mitochondrial sequence of reference ([42]; accession number AF533441). PCR
amplifications were conducted in a 25 µl volume with 2 mM MgCl2, 200 µM of each
dNTP, 1 µM of each primer and 1 unit of AmpliTaq Gold Polymerase (Applied
Biosystems). After a 10 min period at 95°C for polymerase activation, 35 cycles were run
with the following steps: 95°C: 30s, 55°C: 30s, 72°C: 1 min. PCR products were purified
using the Qiaquick PCR purification kit (Qiagen). 35 ng of purified DNA from this PCR
product was used for sequencing with the CAP-F or CAP-R primer. Sequence reactions
were performed for both DNA strands by using the ABI PRISM Dye Terminator Cycle
Sequencing Reaction Kit (Applied Biosystems) in a 20 µl volume with 2 µM of each
primer. 25 cycles were run with the following steps 96°C: 30s, 55°C: 30s, 60°C: 4 min.
Excess dye terminators were removed by spin-column purification and the products were
electrophorezed on an ΑΒΙ 3700 PRISM DNA sequencer (Applied Biosystems) using the
POP 7 polymer.

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Chapter 3 mtDNA diversity of goats

Sequences were edited for correction with the SeqScape v2.5 software (Applied
Biosystems). All sequences were deposited in GenBank (Accession Numbers EF617601-
EF618546, Table 3.2).
Sequences from GenBank and from our dataset were aligned with Mega v3.1 [43],
and then adjusted by eye. For further analyses, we only kept the region used by Luikart et
al. [13] because this is the part of the sequence available for most of the GenBank records,
and also the most informative one. This region is 481 bp long and corresponds to the
positions 15,707 to 16,187 on the Capra hircus reference sequence (mtDNA complete
sequence of C. hircus, Accession number AF533441 [42]). According to the
insertion/deletion events, the analyzed sequences ranged from 481 to 558 bp. For Indian
goats a shorter fragment of 453 bp has been sequenced [15] and the 28 missing nucleotides
were treated as missing data. The alignment of the 2430 sequences used in this study is
provided as supplementary information.

Data analysis

The substitution model used for the HVI region was the Kimura 2-parameters model,
as previously used on several subsets of the present dataset (e.g., [13,15]). The
heterogeneity in substitution rates among nucleotide sites was modelled by a gamma
distribution. The alpha parameter was estimated as the mean of 10 estimations by a
maximum-likelihood method under the Kimura 2-parameters model using PAML v 2.0.2
[44]. Each estimation was based on the analysis of 1000 individuals randomly chosen in
the dataset of 2430 individuals. The estimated value (alpha = 0.28) was similar to that
estimated for the same region on a smaller sample of domestic and wild goats by Luikart
et al. [13]. These settings were used for further phylogenetic reconstruction and analysis of
genetic diversity. We used 1484 published sequences for checking the validity of the
halpogroups previously defined (see Table 3.2 for references and GenBank accession
numbers).
Given the very high number of sequences analyzed, the phylogenetic tree was
constructed using the Neighbor-joining method using PAUP* v 4.0 [45], with 1000
bootstraps for measuring branch robustness. The ARLEQUIN v 3.0 software [46] was
used for estimating haplotype and nucleotide diversity, for analyzing mismatch
distribution within mitochondrial haplogroups, and for estimating the parameters of

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Chapter 3 mtDNA diversity of goats

demographic expansion. Four individuals that showed a 76 bp insertion were discarded for
mismatch analyses and the analyses were thus performed on 481 bp long sequences. The
expansion time was estimated under a model of pure demographic expansion [22] with
parameters set to default values in ARLEQUIN 3.0. The parameter of demographic
expansion τ was estimated according to the method of Schneider and Excoffier [47]. The
validity of the expansion model was tested using the sum of square deviations (SSD)
between the observed and expected mismatches [47].
Growth rates of mitochondrial haplogroups were estimated with Lamarc v2.2 [48]
using a bayesian framework allowing migrations across haplogroups (with a maximum of
10000 migration events, default priors used for migration rates estimation). The estimation
of growth rates was done with linear prior (upper bound of 1000 and lower bound of -
500), 10 initial chains (500 samples, sampling interval of 20 and burn-in period of 1000)
and 2 final chains (10000 samples, sampling interval of 20 and burn-in period of 1000).
In order to test the geographic structure of the mtDNA haplotype diversity, the goat
distribution has been partitioned in 7 geographic regions (Northern Europe, Southern
Europe, Northern Africa, Sub-Saharan Africa, Middle East, Western Asia and Eastern
Asia, see Table 3.2). Two hierarchical AMOVA were performed using ARLEQUIN v3.0
to test the partition of the genetic variance among haplogroups and among continents
within haplogroups, as well as among continents and among breeds within continents.
This second AMOVA was performed on the 1602 goats for which the breeds were known.

Acknowledgements

We would like to thank Prof. Oscar Gaggiotti for fruitful discussions and
constructive comments, Cécile Albert for help with figures, and Jessica Scriven and
Alison Cleary for help with the English. We are grateful to Ebrahim Ghaderi and Prof.
Mahamoud Abo-Shehada for their help for collecting samples in Iran and Jordan. We also
thank two anonymous reviewers for constructive and stimulating comments.

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Chapter 3 mtDNA diversity of goats

References

1. Clutton-Brock J (1999) Domesticated animals from early times. The Natural History
Museum: Cambridge University Press. 238 p.
2. Porter V (1996) Goats of the world. Ipswich, Uk: Farming Press. 172 p.
3. Pringle H (1998) Reading the signs of ancient animal domestication. Science 282: 1448-
1450.
4. Zeder M, Emshwiller E, Smith B, Bradley D (2006) Documenting domestication: the
intersection of genetics and archaeology. Trends Genet 22: 139-155.
5. MacHugh D, Bradley D (2001) Livestock genetic origins: goats buck the trend. Proc
Natl Acad Sci USA 98: 5382-5384.
6. Meadow RH (1996) The Origins and Spread of Agriculture and Pastoralism in
northwestern South Asia. In: Harris DR. The Origins and Spread of Agriculture and
Pastoralism in Eurasia. London: UCL Press. pp. 390-412.
7. Zeder M, Hesse B (2000) The initial domestication of goats (Capra hircus) in the Zagros
Mountains 10,000 years ago. Sciences 287: 2254-2257.
8. Zeder M, Vigne JD, Helmer D (2005) A view from the Zagros: new perspectives on
livestock domestication in the Fertile Crescent. In: Vigne JD, Peters J, Helmer D,
editors. The first steps of animal domestication: Oxbow Books. pp. 125-146.
9. Takada T, Kikkawa Y, Yonekawa H, Kawakami S, Amano T (1997) Bezoar (Capra
aegagrus) is a matriarchal candidate for ancestor of domestic goat (Capra hircus):
evidence from the mitochondrial DNA diversity. Biochem Genet 35(9-10): 315-326.
10. Manceau V, Despres L, Bouvet J, Taberlet P (1999a) Systematics of the genus Capra
inferred from mitochondrial DNA sequence data. Mol Phylogenet Evol 13(3): 504-510.
11. Pidancier N, Jordan S, Luikart G, Taberlet P (2006) Evolutionary history of the genus
Capra (Mammalia, Artiodactyla): discordance between mitochondrial DNA and Y-
chromosome phylogenies. Mol Phylogenet Evol 40: 739-749.
12. Bruford M, Bradley D, Luikart G (2003) DNA markers reveal the complexity of
livestock domestication. Nat Rev Genet 3: 900-910.
13. Luikart G, Gielly L, Excoffier L, Vigne JD, Bouvet J et al. (2001) Multiple maternal
origins and weak phylogeographic structure in domestic goats. Proc Natl Acad Sci
USA 98: 5927-5932.

- 87 -
Chapter 3 mtDNA diversity of goats

14. Sultana S, Mannen H, Tsuji S (2003) Mitochondrial DNA diversity of Pakistani goats.
Anim Genet 34(6): 417-421.
15. Joshi MB, Rout PK, Mandal AK, Tyler-Smith C, Singh L et al. (2004)
Phylogeography and origin of Indian domestic goats. Mol Biol Evol 21(3): 454-462.
16. Chen SY, Su YH, Wu SF, Sha T, Zhang YP (2005) Mitochondrial diversity and
phylogeographic structure of Chinese domestic goats. Mol Phylogenet Evol 37(3): 804-
814.
17. Odahara S, Chung H, Choi S, Yu S, Sasazaki S et al. (2006) Mitochondrial DNA
diversity of Korean native goats. Asian Australas J Anim Sci 19: 482-485.
18. Sardina MT, Ballester M, Marmi J, Finocchiaro R, van Kaam JB et al. (2006)
Phylogenetic analysis of Sicilian goats reveals a new mtDNA lineage. Anim Genet
37(4): 376-378.
19. Amills M, Capote J, Tomas A, Kelly L, Obexer-Ruff G et al. (2004) Strong
phylogeographic relationships among three goat breeds from the Canary Islands. J
Dairy Res 71(3): 257-262.
20. Azor PJ, Monteagudo LV, Luque M, Tejedor MT, Rodero E et al. (2005) Phylogenetic
relationships among Spanish goats breeds. Anim Genet 36(5): 423-425.
21. Pereira F, Pereira L, Van Asch B, Bradley D, Amorim A (2005) The mtDNA
catalogue of all Portuguese autochthonous goat (Capra hircus) breeds: high diversity of
female lineages at the western fringe of European distribution. Mol Ecol 14: 2313-
2318.
22. Rogers A, Harpending H (1992) Population growth makes waves in the distribution of
pairwise genetic differences. Mol Biol Evol 9: 552-569.
23. Howell N, Smejkal CB, Mackey DA, Chinnery PF, Turnbull DM et al. (2003) The
Pedigree Rate of Sequence Divergence in the Human Mitochondrial Genome: There Is
a Difference Between Phylogenetic and Pedigree Rates. Am J Hum Genet 72: 659–670.
24. Denver DR, Morris K, Lynch M, Vassilieva LL, Thomas WK (2000) High Direct
Estimate of the Mutation Rate in the Mitochondrial Genome of Caenorhabditis elegans.
Science 289: 2342.
25. Lambert DM, Ritchie PA, Millar CD, Holland B, Drummond AJ et al. (2002) Rates of
Evolution in Ancient DNA from Adélie Penguins. Science 295: 2270.
26. Bradley D, MacHugh D, Cunningham P, Loftus R (1996) Mitochondrial diversity and
the origins of African and European cattle. Proc Natl Acad Sci USA 93: 5131-5135.

- 88 -
Chapter 3 mtDNA diversity of goats

27. Naderi S, Rezaei HR, Pompanon F, Blum MGB, Negrini R et al. (In Prep.) Genetic
evidence for a large scale domestication in goats.
28. Fumagalli L, Taberlet P, Favre L, Hausser J (1996) Origin and evolution of
homologous repeated sequences in the mitochondrial DNA control region of shrews.
Mol Biol Evol 13: 31-46.
29. Hiendleder S, Lewalski H, Wassmuth R, Janke A (1998) The complete mitochondrial
DNA sequence of the domestic sheep (Ovis aries) and comparison with the other major
ovine haplotype. J Mol Evol 47: 441-448.
30. Meadows JRS, Li K, Kantanen J, Tapio M, Sipos W et al. (2005) Mitochondrial
Sequence Reveals High Levels of Gene Flow Between Breeds of Domestic Sheep from
Asia and Europe. J Hered 96(5): 494–501.
31. Meadows JRS, Cemal I, Karaca O, Gootwine E, Kijas JW et al. (2007) Five Ovine
Mitochondrial Lineages Identified From Sheep Breeds of the Near East. Genetics 175:
1371–1379.
32. Mannen H, Kohno M, Nagata Y, Tsuji S, Bradley DG et al. (2004) Independent
mitochondrial origin and historical genetic differentiation in North Eastern Asian cattle.
Mol Phylogenet Evol 32: 539–544.
33. Freeman AR, Meghan CM, Machugh DE, Loftus RT, Achukwi MD et al. (2004)
Admixture and diversity in West African cattle populations. Mol Ecol 13: 3477–3487.
34. Fernández H, Hugues S, Vigne JD, Helmer D, Hodgins G et al. (2006) Divergent
mtDNA lineages of goats in an Early Neolithic site, far from the initial domestication
areas. Proc Natl Acad Sci USA 103:15375-15379.
35. Vigne J.-D. et al., in Archaeozoology of the Near East IV, Proc. 4th int. Symp.
Archaeozoology of Southwestern Asia and adjacent areas (ASWA; Paris, June 1998)
M. Mashkour, A. M. Choyke, H. Buitenhuis, F. Poplin, Eds. (Archaeological Research
and Consultancy, Groningen, 2000), vol. Publicaties 32, pp. 52-75.
36. Tuñon M, Gonzalez JP, Vallejo M. (1989) Genetic relationships between 14 native
spanish breeds of goat. Anim Genet 20:205-212.
37. Cañon J, García D, García-Atance M, Obexer-Ruff AG, Lenstra J et al. (2006)
Geographical partitioning of goat diversity in Europe and the Middle East. Anim Genet
37:327–334.
38. Pariset L, Cappuccio I, Ajmone Marsan P, Dunner S, Luikart G et al. (2006)
Assessment of population structure by single nucleotide polymorphisms (SNPs) in goat
breeds. J Chromatography B.

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Chapter 3 mtDNA diversity of goats

39. Taberlet P, Ajmone-Marsan P, Valentini A, Rezaei HR, Naderi S et al. (2008) Are
cattle, sheep, and goats endangered species? Mol Ecol 17: 275-284.
40. Luikart G, England P, Tallmon D, Jordan S, Taberlet P (2003) The power and promise
of population genomics: from genotyping to genome typing. Nat Rev Genet 4: 981-994.
41. Shackleton DM (1997) Wild sheep and goats and their relatives: Status survey and
conservation action plan for Caprinae. Gland, Switzerland: IUCN. 390 p.
42. Parma P, Feligini M, Greeppi G, Enne G (2003) The complete nucleotide sequence of
goat (Capra hircus) mitochondrial genome. Goat mitochondrial genome. DNA Seq
14(3): 199-203.
43. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular
evolutionary genetics analysis and sequence alignement. Brief Bioinform 5: 150-163.
44. Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum
likelihood. CABIOS 13: 555-556.
45. Swofford DL (2003) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other
Methods), Version 4. Sinauer Associates, Sunderland, Massachusetts.
46. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software
package for population genetics data analysis. Evolutionary Bioinformatics Online 1:
47-50.
47. Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the
distribution of pairwise differences when the mutation rates vary among sites:
application to human mitochondrial DNA. Genetics 152: 1079-1089.
48. Kuhner M (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of
population parameters. Bioinformatics 22: 768-770.

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Chapter 4. Goat domestication
Chapter 4 Goat Domestication

Chapter 4. Goat domestication: a single large-scale event without

bottleneck

Saeid Naderi,1,2 Hamid-Reza Rezaei,1,3 François Pompanon,1 Michael G. B. Blum,4

Riccardo Negrini,5 Hamid-Reza Naghash,1 Özge Balkız,6 Marjan Mashkour,7 Oscar
Gaggiotti,1 Paolo Ajmone-Marsan,5 Aykut Kence,6 Jean-Denis Vigne,7 Pierre Taberlet,1

1
Laboratoire d'Ecologie Alpine, CNRS UMR 5553, Université Joseph Fourier, BP 53,
38041 Grenoble Cedex 9, France.
2
Natural Resources Faculty of Guilan University, Guilan, Iran.
3
Environmental Sciences Department, Gorgan University of Agriculture and Natural
Resources, Gorgan, Iran.
4
Laboratoire TIMC-IMAG, CNRS, Université Joseph Fourier, Grenoble, 38706 La
Tronche Cedex, France.
5
Istituto di Zootecnica, Università Cattolica del S. Cuore, via E. Parmense, 84, 29100
Piacenza, Italy.
6
Biology Department, Middle East Technical University, 06531, Inonu Bulv. Ankara,
Turkey.
7
CNRS, UMR 5197, Muséum National d'Histoire Naturelle , "Archéozoologie, Histoire
des Sociétés Humaines et des Peuplements Animaux", Département d'Ecologie et Gestion
de la Biodiversité, CP 56, 57 rue Cuvier, 75231 Paris Cedex 05, France.

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Chapter 4 Goat Domestication

The emergence of farming during the Neolithic transition, including the

domestication of livestock, was a critical point in the evolution of humankind.
Together with sheep, cattle and pigs1-3, the goat (Capra hircus) was one of the first
domesticated ungulates. While the precise domestication process remains unknown
in livestock animals, it has been postulated that a strong reduction of population size
- a bottleneck - occurs at the very early phase of domestication4. However, we show
that goat domestication was in fact a large-scale process, without bottleneck. A
comparison based on extensive sampling of goat genetic diversity to that of its wild
ancestor, the bezoar, reveals a two-step scenario for goat domestication. A signature
of population expansion in bezoars bearing mitochondrial DNA (mtDNA) haplotypes
similar to those of goats, suggests an initial phase of management of wild flocks that
fits well with some archaeological proposals. A second phase – the effective
domestication – occurred mainly in Eastern Anatolia, and possibly in Northern and
Central Zagros, and involved the capture of a large number of mtDNA haplotypes.
This scenario strongly differs from previous bottleneck models that saw
domestication occurring within restricted areas with population reductions. Our
results, with their attendant implications for the development of early farming,
should direct future research on animal domestication towards testing if the absence
of bottleneck is the rule or the exception.

The first archaeological evidence of goat domestication traces back as far as ca.
10,500 calibrated Before Present (cal. B.P.) in the high Euphrates and Tigris valleys, in
Southeastern Anatolia5-6 and 9,900-9,500 cal. B.P. in the Zagros mountains3,4,7. While the
hypothesis concerning goat domestication in the Southern Levant8 seems to be more and
more debatable, the domestication of local ungulates, especially goats, in the Lower Indus
valley during the late 8th /early 7th millennia cal. B.P.9 has not yet been contested. It is
now widely recognized that the goat’s wild ancestor is the bezoar, Capra aegagrus10.
The three goat (C. hircus) mtDNA haplogroups (A, B, and C) found by Luikart et
al.11 have been interpreted to signify three distinct domestication events. Assuming a
single haplotype domesticated per haplogroup and a coalescence time of 10,000 years for
the most common A haplogroup, the domestication of B and C haplogroups have been
hypothesised to have occurred about 2130 and 6110 years ago, respectively11. However,
the finding of the C haplogroup dating to 7500 years ago in Southern France12, far from

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Chapter 4 Goat Domestication

putative domestication centres, threw the initial scenario calling for sequential
domestications11 into question. The recent analysis of 2430 goat individuals revealed a
total of six different monophyletic mtDNA haplogroups A, B, C, D, F, and G, with the A
haplogroup representing more than 90% of individuals13.
In this context, our main objective was to better understand the domestication process
by an extensive analysis of the mtDNA polymorphism both in the domestic goat and in its
wild ancestor. More specifically, we aimed to localize the putative domestication centres
by finding the present day wild populations that bear the closest genotypes when
compared to the domestic populations, using extensive and well-controlled sampling in the
field. We also aimed to quantify the amount of mitochondrial and nuclear DNA diversity
captured during the domestication process. Thus we analyzed the mtDNA control region
of 487 modern bezoars from 43 localities covering most of the distribution range (see
Methods and Supplementary Information), and compared it with the polymorphism of the
homologous region in goats (Figure 4.1). Using five breeds from Iran and three from Italy
we also compared the nuclear DNA polymorphism (via AFLP14) between the bezoar and
domestic breeds.
Our first main finding is that bezoars bearing haplotypes close to domestic goats have
had a significantly higher population growth rate, compared to other bezoars (Table 4.1).
This evidence of a population size increase of the domestics’ antecedents, suggests a phase
of sustainable management of some wild flocks of bezoars, probably before true
domestication. Such a population increase fits well with some archaeozoological findings,
which suggest both the "controlling and protecting herds of [wild] caprines"15 and the
subsequent management of animals morphologically indistinguishable from wild
populations7,16, before incipient domestication / population isolation, as defined by
Horwitz17. This phase of "pre-domestication"16 might have lasted several centuries or
millennia, as suggested by some archaeologists specializing in the Near East18. In the
Central Zagros, the “pre-domestic” phase would have been characterized by culling more
young males and older females, which is not the case for hunted bezoars7. Later on,
individuals from these managed bezoar flocks transferred from their natural distribution
area (Figure. 4.2a) would have been the source of fully domestic goats, and may even have
become partly feralized, as they did ca. 10.000 cal. B.P. in Cyprus16,19. Consequently, a
large proportion of the modern bezoar populations might come from herds that were
managed by humans during these early pre-Neolithic and Neolithic periods. Indeed, the
current geographic distribution of bezoars genetically close-to-domestics, with a

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Chapter 4 Goat Domestication

population expansion signature, encompasses a large area that includes Eastern Anatolia,
the whole Zagros, the Central Iranian Plateau, and Northeastern Iran. Thus, the phase of
pre-domestic management was not a local phenomenon, but a widespread practice in
numerous localities spread over an area much larger than suggested by archaeozoology.

Figure 4.1. Phylogenetic relationship of the 251 haplotypes from the 487 bezoars
studied. This tree was obtained with the neighbour joining method (see Methods). In order
to identify shared mtDNA haplogroups, 22 haplotypes chosen to represent the overall
diversity of modern goats13 have also been included in the analysis (in red). The scale
represents the genetic distance. The different colors correspond to the haplotypes from the
different mtDNA haplogroups found in goat (A: green, B: dark blue, C: yellow, D: purple,
F: light blue, G: orange). The other bezoar haplotypes are represented in white.

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Chapter 4 Goat Domestication

Table 4.1. Estimation of population growth rates (most probable estimates) for domestic
goat and for two categories of bezoar (wilds close-to-domestics; wilds non close-to-
domestics) using Lamarc v2.225.

Growth rate 95% percentile

No gene flow with domestics

Domestics 260.73 252.77-268.47

Wilds close-to-domestics 71.11 52.75-81.97

Wilds non close-to-domestics 19.47 13.25-23.62

Gene flow with domestics

Domestics 108.57 95.53-112.59

Wilds close-to-domestics 67.44 59.52-77.59

Wilds non close-to-domestics 29.91 24.27-40.29

The demographic model always considers migration between wild populations. Results
presented in the upper half of the table assume no migration between wilds and domestics.
Results presented in the bottom half assume migration between wilds and domestics. Four
independent runs gave similar results (one run presented). The growth rate given is equal
to g/µ, where g is the parameter governing the exponential growth model used by Lamarc
and µ is the mutation rate.

The phylogeographic structure of the bezoar is weak compared to other wild

ungulates (see e.g. ref. 20), and the same mtDNA haplotypes can be found in very distant
localities (e.g. 1635 km for haplotype 54 found in localities 8 and 28; 3022 km for
haplotype 136 found in localities 6 and 43; etc.). Such a mixing of haplotypes is very
unusual in natural populations (except for animals with high dispersal abilities such as
birds; e.g. ref. 21, 22). The most likely explanation for such a mixing in bezoars is that
humans translocated many animals in the past, probably during the pre-domestication
phase, before morphological modifications. Such a transfer is archaeologically attested in
Cyprus16,19. This mixing is particularly obvious for the C haplogroup that now occupies
almost all of the bezoar distribution area (Figure 4.2b). According to the strong

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Chapter 4 Goat Domestication

predominance of the C haplogroup in Southern Zagros and in the Central Iranian Plateau,
one can hypothesize that these two regions were at the origin of the C haplogroup, and that
the pre-domestication phase began there.

Figure 4.2. Study area and geographic distribution of the mtDNA haplogroups in the
bezoar. a, Natural distribution of the bezoar according to Uerpmann28. This distribution
may not have changed since the beginning of goat management/domestication, and stops
at the Eastern limit of the map. The archaeological sites that give evidence of local pre-
Neolithic goat domestication are represented in red.

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Chapter 4 Goat Domestication

(Figure 4.2, continued) The sites that suggest either local goat domestication or early pre-
pottery Neolithic transfer of domesticated goat are represented in orange. Finally, the sites
that provide evidence of transfer of goats out of the original geographic range of the
bezoar before the middle of the 10th millennium cal. B.P. are represented in yellow
(Supplementary Table 4.3). b, Geographic distribution of the mtDNA haplogroups in the
bezoar. The size of the circles is proportional to the number of individuals analyzed. The
different bezoar haplogroups are color-coded as in Figure 4.1. Different localities are
identified by numbers, as in Supplementary Table 4.1.

Our second main finding deals with the subsequent effective domestication process
that led to morphologically different animals. The large number - dozens or hundreds - of
mtDNA haplotypes captured at this initial step of the effective domestication argues for a
large-scale process (Supporting Information). Such a large number of ancestral goat
haplotypes cannot have come from a geographically restricted area. Again, this suggests a
process that occurred over a wide range and over several centuries, implying that at least
several hundred individuals were taken from the managed populations to initiate domestic
flocks. Finally, the fact that several traditional breeds in Iran have a genetic diversity at
nuclear loci close to or even higher than the current bezoar populations also argues for
very large-scale domestication. Thus, the first domesticated goats were able to capture
most of the genetic diversity of their wild ancestors. Clearly, goats do not fit with the
bottleneck domestication paradigm that has been extensively documented in plants4.
The last significant finding concerns the putative location of the true domestication
centres. Today, 90% of the goat mtDNA haplotypes belong to the A haplogroup, a
proportion which cannot have changed dramatically in the expanding goat population
since domestication. (Supplementary Information). The A haplogroup is missing in
bezoars from the Zagros and from the Iranian Plateau and its presence in the easternmost
locality analyzed in Iran (locality 33, in Figure 4.2b) can be explained by introgression
from goats (Supplementary Information). The most likely origin of the A haplogroup in
goats therefore lies in Eastern Anatolia, where it is common in wild populations. This is
fully consistent with recent archaeological evidence of ca. 10,500 cal. B.P. goat
domestication there (e.g. Nevalı Çori, Figure 4.2a). The C haplogroup has a widespread
geographic distribution in bezoars, but the closest relatives to the domestics are found in

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Chapter 4 Goat Domestication

Eastern Anatolia (Figure 4.3), suggesting that the C haplogroup domestics also originate
from this region.

Figure 4.3. Phylogenetic tree (neighbour joining) of the C haplogroup in both goats
(in red) and bezoar (light green from Eastern Turkey, dark green from other
locations). This tree was obtained with the neighbour joining method (see Methods). The
close relationships between bezoars from Eastern Turkey and goats demonstrates that the
domestication for the C haplogroup occurred in this area. The domestic goat C haplotypes
are grouped into at least three clusters, suggesting at least three ancestral haplotypes. The
numbers represent the populations as in Figure 4.2b and Supplementary Table 4.1.

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Chapter 4 Goat Domestication

The bezoars of the C haplogroup in Eastern Anatolia were probably translocated

from the Southern Zagros or the Central Iranian Plateau during the pre-domestic phase, as
suggested by the presence of the same C haplotype in localities 8 and 28 (Figure 4.2b).The
D haplogroup occupies a wide area in the Zagros, consistent with the second earliest
archaeologically known domestication area, ca. 9,900-9,500 cal. B.P. in Central Zagros7.
Conversely, the rather restricted distribution of the B and G haplogroups in the Northern
Zagros, suggest that goats were also domesticated in this area, which was not indicated by
archaeology. However, it is possible that these different events occurred at different times,
over a long period between the earliest known ungulate domestications, ca. 10,500 cal.
B.P. and the latest neolithisation steps in the Near and Middle East, during the 8th-7th
millennia cal. B.P. Our results do not support the possible domestication centre for goats
in the Lower Indus Valley9.
To summarize, the domestication process in goats was preceded over a large area and
before the 11th millennium B.P., by a period of pre-domestic management of wild flocks
that did not induce any detectable morphological change. This first step led to significant
increases in population sizes that are still detectable today in the bezoar populations. It
seems that Southern Zagros and the Central Iranian Plateau played a key role in this first
phase, and were the source of several trans-located populations with C and D haplogroups.
The second step consisted of the true domestication and occurred in Eastern Anatolia
starting from 11,500 B.P., and possibly in Northern and Central Zagros starting from
10,000 B.P. According to the overrepresentation of the A haplotype in modern goats,
Eastern Anatolia was undoubtedly the main contributor. Dozens of mtDNA haplotypes
were captured, probably corresponding to the early domestication of hundreds of
individuals.
This scenario is very different from previous models, which call for restricted
domestication centres and population bottlenecks. The next challenge will be to test if
such a large-scale scenario without bottlenecks is also applicable to other domestic
animals. Is the absence of bottlenecks during the domestication process a prerequisite for a
successful and sustainable domestication?

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Chapter 4 Goat Domestication

METHODS SUMMARY
Mitochondrial DNA analyses

483 wild goats were sampled from 42 geographic localities representing the whole
distribution area, mostly using a non-invasive approach23 (Supplementary Table 4.1). A
481 bp fragment of the control region (HVI, hypervariable region I) was sequenced as in
ref. 11. These sequences were analyzed using neighbour joining (NJ) methods, Bayesian
(MB) and maximum likelihood (ML). The ARLEQUIN v 3.0 software24 was used to
estimate the percentage of variance among regions and localities by an analysis of
molecular variance (AMOVA) (See Methods).

Estimation of population growth rate

Growth rates of mitochondrial haplogroups were estimated with Lamarc v2.225 using
a bayesian framework (See Methods).

Estimation of the number of goat mtDNA haplotypes captured during the

domestication process

The number of ancestral haplotypes has been estimated using a phylogenetic

approach, assuming a domestication time between 13,000 and 9,000 years B.P., and a
divergence time of 200 to 300 thousand years between goat haplogroups A and C11. To
infer how many goat haplotypes would be found in a sample containing any possible
number of sequences, we performed a rarefaction analysis. We also computed the pairwise
coalescence times for all pairs of domestic and wild sequences. Finally, assuming a neutral
model of evolution, we computed the minimum frequency of the goat A haplogroup at the
domestication time (See Methods).

Nuclear DNA analysis

A total of 232 goats (five breeds from Iran and three breeds from Italy) were
analyzed, and compared with 19 bezoar samples, using AFLP markers according to the
protocol described in Ajmone-Marsan et al.26 (Supplementary Table 4.2). The amount of
genetic variation within each goat breed and within the bezoar population was estimated
by averaging Jaccard similarity between individuals belonging to the same breed or
population27 (See Methods).

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Chapter 4 Goat Domestication

1. Harris, D. R. The Origins and Spread of Agriculture and Pastoralism in Eurasia.

(Smithsonian Institution Press, Washington D.C., 1996).

2. Vigne, J.-D., Peters, J. & Helmer, D. The First Steps of Animal Domestication. New
Archaeological Approaches. (Oxbow Books, Oxford, UK, 2005).

3. Zeder, M. A. & Hesse, B. The initial domestication of goats (Capra hircus) in the
Zagros Mountains 10,000 years ago. Science 287, 2254-2257 (2000).

4. Zeder, M. A., Emshwiller, E., Smith, B. D. & Bradley, D. G. Documenting

domestication: the intersection of genetics and archaeology. Trends Genet. 22, 139-
155 (2006).

5. Peters, J., Helmer, D., von den Driesch, A. & Saña-Segui, M. Early animal
husbandry in the Northern Levant. Paléorient 25, 27-48 (1999).

6. Peters, J., von den Driesch, A. & Helmer, D. in The First Steps of Animal
Domestication. New Archaeological Approaches (eds Vigne, J.-D., Peters, J. &
Helmer, D.) 96-124 (Oxbow Books, Oxford, UK, 2005).

7. Zeder, M. A. in The First Steps of Animal Domestication. New Archaeological

Approaches (eds Vigne, J.-D., Peters, J. & Helmer, D.) 125-146 (Oxbow Books,
Oxford, UK, 2005).

8. Horwitz, L. K. et al. Animal domestication in the Southern Levant. Paléorient 25,

63-80 (2000).

9. Meadow, R. H. in The Origins and Spread of Agriculture and Pastoralism in

Eurasia (ed Harris, D. R.) 390-412 (Smithsonian Institution Press, Washington D.C.,
1996).

10. Manceau, V., Després, L., Bouvet, J. & Taberlet, P. Systematics of the Capra genus
inferred from mitochondrial DNA sequence data. Mol. Phyl. Evol. 13, 504-510
(1999a).

11. Luikart, G. et al. Multiple maternal origins and weak phylogeographic structure in
domestic goats. Proc. Natl. Acad. Sci. USA 98, 5927-5932 (2001).

12. Fernández, H. et al. Divergent mtDNA lineages of goats in an Early Neolithic site,
far from the initial domestication areas. Proc. Natl. Acad. Sci. USA 103, 15375-
15379 (2006).

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Chapter 4 Goat Domestication

13. Naderi, S. et al. Large-scale mitochondrial DNA analysis of the domestic goat
reveals six maternal lineages with high haplotype diversity. PLoS ONE, (2007),
2(10): e1012.

14. Vos, P. et al. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23,
4407-4414 (1995).

15. Hole, F. in The Origins and Spread of Agriculture and Pastoralism in Eurasia (ed
Harris, D. R.) 263-281 (Smithsonian Institution Press, Washington D.C., 1996).

16. Vigne, J.-D. et al. in Archaeozoology of the Near East IV, Proc. 4th int. Symp.
Archaeozoology of Southwestern Asia and Adjacent Areas (ASWA; Paris, June
1998) (eds Mashkour, M., Choyke, A. M., Buitenhuis, H. & Poplin, F.) 52-75
(Archaeological Research and Consultancy, Groningen, 2000).

17. Horwitz, L. K. in People and Culture in Change (Proc. 2nd Symp. On Upper
Palaeolithic, Mesolithic and Neolithic of Europe and the Mediterranean Basin) (ed
Hershkovitz, I.) 153-181 (Part i. British Archaeol. Rep., Int. Ser. Vol. 508, 1989).

18. Legge, A. J. in Papers in economic prehistory (ed Higgs, E. S.) 119-124 (Cambridge
University Press, Cambridge, 1972).

19. Vigne, J.-D., Carrère, I. & Guilaine, J. in Le Néolithique de Chypre (eds Guilaine, J.
& Le Brun, A.) 239-251 (Bull. Corr. Hélléniques, Vol. Suppl. 43, 2003).

20. Zhang, F. F. & Jiang, Z. G. Mitochondrial phylogeography and genetic diversity of

Tibetan gazelle (Procapra picticaudata): Implications for conservation. Mol. Phyl.
Evol. 41, 313-321 (2006).

21. Questiau, S., Gielly, L., Clouet, M. & Taberlet, P. Phylogeographic evidence of gene
flow among Common Crossbill populations at the continental level (Loxia
curvirostra, Aves, Fringillidae). Heredity 83, 196-205 (1999).

22. Ball, R.M. et al. Phylogeographic population structure of Red-winged Blackbirds

assessed by mitochondrial DNA. Proc. Natl. Acad. Sci. USA 85, 1558-1562 (1988).

23. Taberlet, P., Waits, L.P. & Luikart, G. Noninvasive genetic sampling: look before
you leap. Trends Ecol. Evol. 14, 321-325 (1999).

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Chapter 4 Goat Domestication

24. Excoffier, L., Laval, G. & Schneider, S. Arlequin (version 3.0): an integrated
software package for population genetics data analysis. Evol. Bioinformatics Online
1, 47-50 (2005).

25. Kuhner, M. K. LAMARC 2.0: maximum likelihood and Bayesian estimation of

population parameters. Bioinformatics 22, 768-770 (2006).

26. Ajmone-Marsan, P. et al. AFLPTM markers for DNA fingerprinting in cattle. Anim.
Genet. 28, 418-426 (1997).

27. Jaccard, P. Nouvelles recherches sur la distribution florale. Bull. Soc. Vaud. Sci. Nat.
44, 223-270 (1908).

28. Uerpmann, H.-P. The Ancient Distribution of Ungulate Mammals in the Middle
East. (Dr Ludwig Reichert Verlag, Wiesbaden, 1987).

Figure 4.4. Capra aegagrus in Golestan National Park in Iran (Photo by HR. Rezaei).

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Chapter 4 Goat Domestication

Acknowledgements

We would like to thank Dr. Bahram Kiabi, Ramezanali Ghaemi and Bijan Farhang
Darehshoori for fruitful discussions and constructive comments. We also thank the Iranian
Departement of Environment for sampling authorizations (Nb 13/1-36694-1383), and
Javad Ramezani and Afshin Karami for their administrative support. We are gratefull to
all the guards of National Parks and other protected areas, and to Ebrahim Ghaderi, Rasul
Marsooli, Seyed Abbas Rafat, Paul Weinberg, Amjad Tahir Virk, and Gordon Luikart for
their help during the field sampling in Iran, Azerbaijan, Dagestan and Pakistan. Thanks are
due to the Turkish General Directorate of Nature Protection and National Parks for their
cooperation during the field sampling as well. J.-D. Vigne benefited from grants from the
ESF OMLL project “Early Bovids” for archaeological field sessions. We greatly
appreciated the help of Delphine Rioux, Stéphanie Zundel, Ludovic Gielly, Christian
Miquel, and Carole Poillot in the Grenoble laboratory. We thank G.W. Hewitt, R.
Geremia, P. Choler and L. Després for their critical reading of the manuscript. S. Naderi
and HR. Rezaei were supported by PhD scholarships from the Iranian Ministry of Science,
Research, and Technology (number 800125 and, 791135 respectively). F. Pompanon was
supported by the Institut National de la Recherche Agronomique.

Author information DNA sequences have been deposited at GenBank/EMBL under

accession numbers EF989163-EF989645 (see also Supplementary Information). Reprints
and permissions information are available at [Link]/reprints. The authors
declare no competing financial interests. Correspondence and requests for materials should
be addressed to P.T. (e-mail: [Link]@[Link]).

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Chapter 4 Goat Domestication

METHODS
Mitochondrial DNA analyses

Sampling
Fresh faeces were collected in the field, after observation of the goats from a distance
to ensure the species origin of the sample. For each individual two samples were collected
and preserved with two methods (silica gel and ethanol 96%). Moreover, some samples
consisted of skin and muscle obtained from hunter kills and carcasses. Because of possible
hybridization in captivity, no samples from zoos were considered in this study. In addition
to the samples collected in the field, we retrieved four sequences of C. aegagrus from
GenBank. For comparison with domestic goat, the data set was completed with 22
reference sequences of the mtDNA control region of different haplogroups of C. hircus13.
All C. aegagrus samples used for the mtDNA analysis are listed in Supplementary Table
4.1.

DNA extraction
The whole genomic DNA was extracted from fecal samples after 20 minutes in
washing buffer (Tris-HCl 0.1 M, EDTA 0.1 M, NaCl 0.1 M, N-lauroyl sarcosine 1%,
pH 7.5-8.0), using DNAeasy extraction blood kit (Qiagen) following the manufacture's
protocol for animal blood except for the incubation with protease (2 hours at 56° C with
55 µl of protease). For tissue samples, total DNA was extracted using the tissue extraction
kit QIAamp Animal Tissue kit (Qiagen) following the manufacture's instructions.

DNA amplification
A 598 bp fragment was amplified using the primers CAP-F (5’-
CGTGTATGCAAGTACATTAC-3’)and CAP-R (5’-CTGATTAGTCATTAGTCCATC-
3’). PCR amplifications were conducted in a 25 µl volume with 2 mM MgCl2, 200 µM of
each dNTP, 1 µM of each primer and 1 unit of AmpliTaq Gold Polymerase (Applied
Biosystems). After a 10 min period at 95°C for polymerase activation, 35 cycles for tissue
samples and 40 cycles for faeces samples were run with the following steps: 95°C: 30 sec,
55°C: 30 sec, 72°C: 1 min.

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Chapter 4 Goat Domestication

DNA sequencing
PCR products were purified using the Qiaquick PCR purification kit (Qiagen). 35 ng
of purified DNA from this PCR product was used for sequencing with the CAP-F/CAP-R
primer pair. Sequence reactions were performed for both DNA strands by using the ABI
PRISM Dye Terminator Cycle Sequencing Reaction Kit (Applied Biosystems) in a 20 µl
volume with 2 µM of each primer. 25 cycles were run with the following steps 96°C:
30 sec, 55°C: 30 sec, 60°C: 4 min. Excess dye terminators were removed by spin-column
purification and the products were electrophorezed on an ΑΒΙ 3700 PRISM DNA
sequencer (Applied Biosystems) using the POP 7 polymer.
Sequences were edited for correction with the SeqScape v2.5 software (Applied
Biosystems), were aligned with Mega v3.129, and adjusted by eye when relevant. For
further analyses, we only kept the region used by Luikart et al.11 because this informative
region is available for most of the GenBank records. This region is 481 bp long on the C.
hircus reference sequence (mtDNA complete sequence of C. hircus30, Accession number
AF533441). According to the insertion/deletion events, the analyzed sequences ranged
from 481 to 558 bp. All sequences were deposited in GenBank (Acc. Numbers EF989163-
EF989645, Supplementary Table 4.1).

Data analysis
The substitution model used was the Kimura 2-parameters (K2P) model. The
heterogeneity in substitution rates among nucleotide sites was modelled by a gamma
distribution. The alpha parameter was estimated by a maximum-likelihood method under
the K2P model using PAML v 2.0.231. The estimated value (α = 0.29) was similar to that
estimated for the same region on a smaller sample of domestic and wild goats11. These
settings were used for further phylogenetic reconstruction and analysis of genetic
diversity.
Data were analyzed using neighbour joining (NJ) methods, Bayesian (MB) and
maximum likelihood (ML). Bayesian analyses were performed using MrBayes V3.1.232.
The Markov Chain Monte Carlo search was run with 3x106 generations (repeated three
times), sampling the Markov chain every 100 generations, with a burn-in of 10,000 trees
(as detected by plotting the log likelihood scores against generation number). The most
appropriate likelihood model was determined using the Akaike Information Criterion
implement in ModelTest 3.0733. ML analyses were first performed with PHYML 2.4.434,
using a K2P model of sequence evolution. Using the best tree found by PHYML as a

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Chapter 4 Goat Domestication

starting tree, heuristic ML searches were executed with PAUP* 4.0b1035, with a tree
bisection reconnection (TBR) branch swapping, and all parameter values estimated. Clade
stability was estimated by non-parametric bootstrapping in 100 replicates with PHYML.
NJ36 trees constructed by using MEGA v.3.129. We chose the K2P distance matrix37; the
robustness of each branch was determined by a nonparametric bootstrap test with 1000
replicates and a TBR branch swapping algorithm. The tree topologies obtained with the
different phylogenetic methods are very similar, and only the neighbour-joining result is
presented in Figure 4.1.
The AMOVA24 has been performed on 487 wild individuals from the 43 populations
divided into 8 geographic regions (Eastern Anatolia, Northern Zagros and Caucasus : 6, 7,
8, 9, 10,11, 12, 15, 16; Central Anatolia: 1, 2, 3, 4, 5 ; Albroz and Turkmenistan: 17, 20,
21, 34, 35, 36, 37, 38, 39, 40; Central Zagros : 13, 14, 18, 19; Southern Zagros : 23, 24,
25, 26; Central Iranian Plateau : 22, 27, 28, 29, 30, 31; Eastern Iranian Plateau : 32, 33;
Lower Indus Valley : 41, 42, 43; population numbers refer to Figure 4.2b and
Supplementary Table 4.1).

Estimation of population growth rate

LAMARC v2.225 was implemented either allowing migrations across haplogroups
(with a maximum of 10000 migration events; default priors used for migration rate
estimations), or without migrations. The estimation of growth rates was done with a flat
prior (upper bound of 1000 and lower bound of -500), 10 initial chains (500 samples,
sampling interval of 20 and burn-in period of 1000) and 2 final chains (10000 samples,
sampling interval of 20 and burn-in period of 1000).

Estimation of the number of goat mtDNA haplotypes that were captured during the
domestication process

Phylogenetic approach
A phylogenetic method was used for estimating the number of ancestral haplotypes
leading to the 2427 mtDNA sequences carried by the goats today. The phylogeny of the
2427 goat sequences was reconstructed using the software PHYML 2.4.434 assuming the
HKY85 model of substitution. Heterogeneity of mutation rate across sites was captured by
a gamma distribution with shape parameter 0.2911. We used the software PATHD838 to
create an ultrametric tree from the phylogeny.

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Chapter 4 Goat Domestication

Rarefaction analysis of the number of goat mtDNA haplotypes found according to

the number of samples analyzed
In order to infer how many haplotypes would be found in a sample containing any
possible number of sequences, we performed a rarefaction approach. For different values b
of the number of sequences, we sampled at random b sequences among the 2427
sequences and we computed the ancestral number of haplotypes from the ultrametric tree
obtained from PATHD838. Extrapolation was then performed using polynomial regression
as implemented in the R routine loess ([Link]

Estimation of the Time to the Most Recent Common Ancestor (TMRCA) for the
different goat haplogroups
The estimates of the TMRCA for the different haplogroups were obtained from the
ultrametric tree inferred with PATHD838 (see above).

Computation of the pairwise coalescence times

For all pairs of domestic and wild sequences we computed the genetic distances
defined as the number of site differences. Genetic distances were then rescaled into
coalescence times by calibrating the median distance between the A haplogroup and the C
haplogroup at 250,000 years11.

Frequency of the A haplogroup at the time of the domestication

Assuming a neutral model of evolution, we computed the minimum frequency of the
A haplogroup at the domestication time compatible with its present frequency. More
precisely, we computed the probability of observing more individuals from the A
haplogroup than the number of individuals that have actually been sampled (2208). This
probability was computed for different values of the frequency x of A haplotypes at the
time of the domestication. The smallest frequency value x such that the probability was
larger than 0.01 was considered to be the smallest number of haplotypes captured that is
compatible with the observed number of A haplotypes that have been sampled.
For a given value k of the number of individuals from the A haplogroup at the time
of the domestication and a given value m of the number of ancestral haplotypes, the
proportion of the number of individuals from the A haplogroup at the present time can be
approximated by a Beta distribution with parameters k and m-k. Therefore, the number of
individuals from the A haplogroup today follows a Beta Binomial distribution39 with
parameters k, m-k and n (=2427; the number of individuals analyzed today). The ancestral

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Chapter 4 Goat Domestication

number of individuals from the A haplogroup k is unknown and its distribution is a

binomial with parameters m and x. As a consequence the probability of getting more than
2208 individuals from the A haplogroup today was given by the survival function of the
Beta Binomial distribution integrated over the possible values for the number of ancestral
A haplotypes.

Nuclear DNA analysis

Sampling
The list of samples is given in Supplementary Table 4.2.

DNA extraction
DNA was extracted with the GenElute Mammalian Genomic DNA miniprep kit
[Sigma G1N-70], following the instruction supplied by the manufacturer. DNA quality
and concentration were visually checked by electrophoresis on 1% agarose gel stained
with ethidium bromide.

AFLP procedure
EcoRI/TaqI AFLP molecular markers were produced according to the protocol
described in Ajmone Marsan et al.26. Three highly polymorphic primer pairs carrying
ACA/ACT, ATA/AAG and ATG/AAC as selective nucleotides were assayed on all
animals sampled. AFLP polymorphisms were visually scored as dominant markers, coding
1 the presence and 0 the absence of the band.

Data analysis.
Allele frequencies of each marker were estimated in each population using a
Bayesian approach with uniform distribution of allele frequencies (AFLP-surv 1.040;
[Link] Following this method, the frequency
of the null allele at each locus is computed on the basis of two parameters: sample size and
number of individuals that lack the AFLP fragment. Allele frequencies were used to
calculate summary statistics, as the percentage of polymorphic loci laying within the
frequency range 0.05 to 0.95 and the unbiased average expected heterozygosity41,
assuming Hardy-Weinberg equilibrium. Statistical significance of differences between
population expected heterozygosity values was tested by Kruskal Wallis non-parametric
test.

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Chapter 4 Goat Domestication

The genetic relationship between individuals was investigated by Factorial

Correspondence Analysis (FCA) using the software Genetix v4.0542. FCA43 is a
multivariate method for the analysis of categorical variables analogous to the Principal
Components Analysis. It allows the simultaneous representation of OTUs and loci as a
cloud of points in a metric space. Axes are independent and are ranked according to
fractions of information explained. Inertia, or dispersion, measures this information. The
direction of maximum inertia is the direction in which the cloud of points is most
scattered.
The amount of genetic variation within populations was estimated by averaging
Jaccard similarity27 between individuals belonging to the same population. Variation in
Mantel test generated by Monte Carlo resampling procedures was used to test the
significance of the difference between population Jaccard values (MANTEL-STRUCT
software44, [Link]

29. Kumar, S, Tamura, K, & Nei, M MEGA3: integrated software for molecular
evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics
5, 150-163 (2004).

30. Parma, P, Feligini, M, Greeppi, G, & Enne, G The complete nucleotide sequence of
goat (Capra hircus) mitochondrial genome. DNA Seq. 14, 199-203 (2003).

31. Yang, Z PAML: a program package for phylogenetic analysis by maximum

likelihood. CABIOS 13, 555-556 (1997).

32. Huelsenbeck, J. P. & Ronquist, F. MRBAYES: Bayesian inference of phylogenetic

trees. Bioinformatics 17, 754-755 (2001).

33. Posada, D & Crandall, K A Modeltest: testing the model of DNA substitution.
Bioinformatics 14, 817-818 (1998).

34. Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large
phylogenies by maximum likelihood. Syst. Biol. 52, 696-704 (2003).

35. Swofford, D L PAUP*: phylogenetic analysis using parsimony (*and other

methods), Version 4 (Sinauer Associates, Sunderland, Massachusetts, 1998).

36. Saitou, N. & Nei, M. The neighbor-joining method : a new method for
reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425 (1987).

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Chapter 4 Goat Domestication

37. Kimura, M. A simple method for estimating evolutionary rate of base substitution
through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111-120
(1980).

38. Britton, T et al. Estimating divergence times in large phylogenetic trees. Syst. Biol.,
in press (2007).

39. Johnson, L N, Kotz, S, & Kemp, A W Univariate Discrete Distributions, 2nd

Edition. (John Wiley & Sons, New York, 1992).

40. Vekemans, X., Beauwens, T., Lemaire, M., & Roldan-Ruiz, I. Data from amplified
fragment length polymorphism (AFLP) markers show indication of size homoplasy
and of a relationship between degree of homoplasy and fragment size. Mol. Ecol. 11,
139-151 (2002).

41. Nei, M. Molecular Evolutionary Genetics. (Columbia University Press, New York,
NY, 1987).

42. Belkhir, K et al. GENETIX 4.05, logiciel sous Windows TM pour la génétique des
populations (Laboratoire Génome, Populations, Interactions, CNRS UMR 5000,
Université de Montpellier II, Montpellier (France), 2004).

43. Benzécri, J P L'Analyse des Données, 2.L'Analyse des Correspondances. (Dunod,

Paris, 1973).

44. Miller, M. P. MANTEL-STRUCT: A program for the detection of population

structure via Mantel tests. J. Hered. 90, 258-259 (1999).

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Chapter 4 Goat Domestication

SUPPLEMENTARY INFORMATION

Supplementary results
Partitioning of the mtDNA genetic variance within and among localities
The total genetic variation was distributed within populations (52.90 %) and among
populations within a geographic region (37.70 %). Only 9.40 % of the diversity was
distributed among regions, which reflects the low phylogeographic structure in bezoars
(Supplementary Table 4.4).

Estimation of the number of goat mtDNA haplotypes that have been captured during
the domestication process

Phylogenetic approach
Using 200 to 300 thousand years as the divergence time between A and C
haplogroups1, we found that the number of ancestral haplotypes of the 2427 sequences, at
the domestication time, ranges from 1308 to 1900. The domestication was assumed to
occur between 9,000 and 13,000 years B.P.
Another calibration based on the fact that the C haplogroup has been found in
Southern France 7500 years ago2 can be carried out, assuming that the C haplogroup
comes from the domestication of a single haplotype, and assuming that its domestication
occurred either 7500 or 9500 years ago. When the TMRCA of the C haplogroup was fixed
at 7500 years B.P., we found 12 ancestral haplotypes 9500 years ago for the whole goat
dataset, and 10 ancestral haplotypes 10500 years ago. Obviously, these estimates
correspond to an important underestimation of the number of ancestral haplotypes,
because first the C haplogroup had been domesticated before 7500 years B.P., and second
because several C haplotypes have probably been domesticated, as suggested by the
clustering of domestic goat C haplotypes into at least three clusters within the bezoar
phylogeny (Figure 4.3).
When the TMRCA of the C haplogroup was fixed at 9500 years B.P. (a more
realistic date allowing the spread of the C haplogroup from the domestication area to
Southern France), we found 103 ancestral haplotypes 9500 years ago and 16 ancestral
haplotypes 10500 years ago. Again, if several C haplotypes had been domesticated, this
corresponds to an underestimate.

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Chapter 4 Goat Domestication

Rarefaction analysis of the number of goat mtDNA haplotypes found according to

the number of samples analyzed.
The results are displayed in Supplementary Figure 4.1 and demonstrate that
analyzing more samples would lead to an increase of the estimated number of ancestral
haplotypes.

Estimation of the TMRCA for the different goat haplogroups

Results are presented in Supplementary Table 4.5.

Computation of the pairwise coalescence times.

The proportion of pairs of sequences that coalesced more recently than 13,000 years
ago (an upper bound for the domestication time) is smaller than 1% (Supplementary
Figure 4.2). When using a divergence time of 200,000 years or 300,000 years, the
proportion of pairs of sequences that coalesced before the domestication remained smaller
than 1%. When the calibration was done using a mtDNA control region mutation rate of
2.5*106 site/generation as it has been found in humans3, we found that only 2.5% of the
pairs coalesced before 13,000 years. When using other genetic distances, the proportion of
pairs that coalesced more recently than the domestication remains similar (Results not
shown).

Frequency of the A haplogroup at the time of the domestication.

It is highly unlikely that the frequency of individuals from the A haplogroup at the
time of domestication was below 0.87 (Supplementary Figure 4.3).

Nuclear DNA analysis

The results of the AFLP analysis of eight breeds of domestic goats, compared with
the bezoar are presented on Supplementary Figure 4.4.

Supplementary Discussion
Introgression from the domestics to the wilds in southeastern Iran
Mitochondrial DNA introgression from the domestics to the wilds might make the
current results difficult to interpret. It is therefore important to identify such events in our
dataset. Currently, individuals from the A haplogroups represent 90.86 % of domestic
goats. This proportion cannot have dramatically changed since their domestication, and
thus the A haplogroups were always the most numerous during goat history (see above

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Chapter 4 Goat Domestication

section "Frequency of the A haplogroup at the time of the domestication"). As a

consequence, if an introgression occurred from the domestic to the wild, it should have
mainly concerned the A haplogroup. Furthermore, the introgressed haplotypes should be
expected to appear in many clades of the phylogenetic tree of the A haplogroup, as would
do the A haplotypes of a goat population today. On the contrary, a wild population without
introgression should only show a very limited number of clustered haplotypes.
As the A haplogroup is absent in bezoars from the Iranian Plateau and from the
Zagros, we can deduce that no mtDNA introgression from the domestics to the wilds
occurred in these areas. However, the situation is very different in Lar Mountains (Sistan
Province, Southeast Iran, locality 33 in Figure 4.2b). The bezoar haplotypes of the A
haplogroups in this locality are distributed among many clades of the phylogeny of the A
haplogroup (Supplementary Figure 4.5). This is a strong indication that the bezoars from
this region have been heavily introgressed by goats. As a consequence, we cannot take
into account Lar Mountains as the possible origin of the A haplogroup in goats. This
introgression is also supported by a phylogeographic argument. The phylogenetic tree of
the bezoar (Fig. 4.1) is composed of three main groups: (i) haplogroups non close-to-
domestics and F, (ii) haplogroup C, (iii) haplogroups A, B, D, G. Individuals from
haplogroups A, B, D, and G are clustered together in the phylogenetic tree, and thus are
supposed to be geographically close. Clearly, the only individuals of the A haplogroup that
are not consistent with their position in the phylogeny are in localities 33, 38, and 39.
These introgressions occurred after the effective domestication and thus concerned the
most frequent A haplogroup in goats.

Number of mtDNA haplotypes captured during the domestication process

Luikart et al.1 estimated that the domestication of the C haplogroup occurred around
6, 000 years ago, assuming both a similar and limited amount of mtDNA diversity within
each founder haplogroup, and a domestication of the A haplogroup 10,000 years ago. The
origin of the C haplogroup 6,000 years ago is impossible because domestic goats from this
haplogroup were already present in Europe about 1,500 years earlier. The mtDNA analysis
of bones from an Early Neolithic site from Southwestern Europe showed that at least two
distinct haplotypes from each of the A and C haplogroups were present in this site 7,500
years ago2. This finding demonstrates that the effective domestication of the C haplogroup
is much more ancient. It occurred in the same area (Eastern Anatolia) than the A

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Chapter 4 Goat Domestication

haplogroup, and most probably at the same time. Therefore, this contradicts the
assumption that each haplogroup in goats originated from a single bezoar haplotype.
All our results are concordant with the domestication of large number of goat
individuals. A first set of arguments suggests that most of the present mtDNA diversity
observed in goats already existed at the beginning of the domestication process. The
estimation of the TMRCA for the main different goat haplogroups is more ancient than the
time of domestication (Supplementary Table 4.5), and very few pairs of sequences (less
than 1%) coalesced more recently than 13,000 years ago (an upper bound for the
domestication time). Moreover, the fact that the same haplotype is found in bezoars in
very distant locations even today supports a very low number of mutations since the
domestication. Such translocations probably occurred during the pre-domestication phase,
as it does not make sense to translocate wild animals after the goats have been effectively
domesticated. A second set of arguments posits that the domestication process may have
caught a large amount of genetic diversity by capturing a large number of individuals.
Several methods have been used for estimating the number of ancestral haplotypes that
were captured. The less realistic hypothesis for calibrating the method (i.e., assuming the
domestication of a single C haplotype 7,500 years ago) gave 10 ancestral haplotypes for
the present goat dataset. This estimate is clearly an important underestimation (see
additional results). More realistic assumptions lead to an estimation of more than 1,000
domesticated haplotypes. A rarefaction analysis showed that finding new domestic
haplotypes would increase the estimated number of ancestral haplotypes.
To summarize, both our mtDNA and nuclear DNA results, are consistent with the
capture of a large genetic diversity during the goat domestication process, with no
bottleneck. While bottleneck during domestication has been extensively documented in
plants4, it does not fit with the genetic data available in goats. This might not be an
exception as the capture of a high genetic variability has already been shown in yak5 and
horse6.

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Chapter 4 Goat Domestication

Supplementary Tables and Figures

Supplementary Table 4.1. Geographic origin and characteristics of the wild goat samples for mt-DNA sequence study.

Sample Type
Haplogroup
Haplotypes

Population

Longitude

Accession
Collector
Latitude
Country

Number
number
Sample

Species
Code

(N)
(E)
1 Ca001 1 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989163
2 Ca002 2 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989164
3 Ca003 17 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989165
4 Ca004 3 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989166
5 Ca005 4 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989167
6 Ca006 5 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989168
7 Ca007 6 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989169
8 Ca008 7 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989170
9 Ca009 8 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989171
10 Ca010 9 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989172
11 Ca011 10 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989173
12 Ca012 11 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989174
13 Ca013 12 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989175
14 Ca014 11 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989176
15 Ca015 13 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989177
16 Ca016 14 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Tissue S. Naderi EF989178
17 Ca017 15 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Tissue S. Naderi EF989179
18 Ca018 16 A C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Feces S. Naderi EF989180
19 Ca019 17 A C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989181

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Chapter 4 Goat Domestication

20 Ca020 18 A C. aegagrus Iran Tandooreh (39) 58.87 37.41 Tissue S. Naderi EF989182
21 Ca021 19 A C. aegagrus Turkey Artvin (9) 41.49 41.11 Tissue A. Kence EF989183
22 Ca022 15 A C. aegagrus Turkey Tunceli (8) 39.34 39.07 Tissue A. Kence EF989184
23 Ca023 15 A C. aegagrus Turkey Tunceli (8) 39.34 39.07 Tissue A. Kence EF989185
24 Ca024 15 A C. aegagrus Turkey Tunceli (8) 39.34 39.07 Tissue A. Kence EF989186
25 Ca025 20 A C. aegagrus Turkey Tunceli (8) 39.34 39.07 Bone A. Kence EF989187
26 Ca026 21 A C. aegagrus Turkey Tunceli (8) 39.34 39.07 Bone A. Kence EF989188
27 Ca027 22 A C. aegagrus Turkey Gaziantep (7) 37.72 38.45 Liver A. Kence EF989189
28 Ca028 23 A C. aegagrus Turkey Sumbul (11) 43.78 37.53 Tissue A. Kence EF989190
29 Ca029 24 A C. aegagrus Turkey Gaziantep (7) 37.72 38.45 Tissue A. Kence EF989191
30 Ca030 25 B C. aegagrus Iran Marakan (12) 45.24 38.85 Feces HR. Rezaei EF989192
31 Ca031 26 B C. aegagrus Iran Ghorveh (18) 47.82 35.06 Feces HR. Rezaei EF989193
32 Ca032 27 B C. aegagrus Iran Ghorveh (18) 47.82 35.06 Feces HR. Rezaei EF989194
33 Ca033 26 B C. aegagrus Iran Ghorveh (18) 47.82 35.06 Feces HR. Rezaei EF989195
34 Ca034 28 B C. aegagrus Iran Ghorveh (18) 47.82 35.06 Feces HR. Rezaei EF989196
35 Ca035 29 B C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989197
36 Ca036 30 B C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989198
37 Ca037 31 B C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989199
38 Ca038 32 B C. aegagrus Turkey Van (10) 43.22 38.29 Tissue A. Kence EF989200
39 Ca039 33 B C. aegagrus Turkey Antalya (2) 30.95 36.9 Feces A. Kence EF989201
40 Ca040 34 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989202
41 Ca041 34 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989203
42 Ca042 34 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989204
43 Ca043 34 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989205
44 Ca044 34 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989206
45 Ca045 34 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989207
46 Ca046 35 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989208
47 Ca047 36 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989209
48 Ca048 36 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989210
49 Ca049 36 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989211
50 Ca050 36 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989212
51 Ca051 55 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989213

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Chapter 4 Goat Domestication

52 Ca052 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Tissue S. Naderi EF989214
53 Ca053 37 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989215
54 Ca054 37 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989216
55 Ca055 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989217
56 Ca056 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989218
57 Ca057 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989219
58 Ca058 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989220
59 Ca059 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989221
60 Ca060 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989222
61 Ca061 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989223
62 Ca062 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989224
63 Ca063 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989225
64 Ca064 37 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989226
65 Ca065 38 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989227
66 Ca066 39 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989228
67 Ca067 40 C C. aegagrus Iran Bavanat (25) 53.91 30.31 Feces S. Naderi EF989229
68 Ca068 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989230
69 Ca069 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989231
70 Ca070 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989232
71 Ca071 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989233
72 Ca072 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989234
73 Ca073 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989235
74 Ca074 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989236
75 Ca075 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989237
76 Ca076 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989238
77 Ca077 42 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989239
78 Ca078 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989240
79 Ca079 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989241
80 Ca080 41 C C. aegagrus Iran Khabr (31) 56.48 28.84 Tissue S. Naderi EF989242
81 Ca081 43 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989243
82 Ca082 44 C C. aegagrus Iran Malayer (19) 48.95 34.21 Feces HR. Rezaei EF989244
83 Ca083 45 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989245

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Chapter 4 Goat Domestication

84 Ca084 45 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989246
85 Ca085 45 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989247
86 Ca086 45 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989248
87 Ca087 45 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989249
88 Ca088 46 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989250
89 Ca089 46 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989251
90 Ca090 46 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989252
91 Ca091 46 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989253
92 Ca092 47 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989254
93 Ca093 48 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989255
94 Ca094 48 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989256
95 Ca095 48 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989257
96 Ca096 49 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989258
97 Ca097 50 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989259
98 Ca098 51 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989260
99 Ca099 52 C C. aegagrus Iran Khartooran (36) 55.86 35.77 Feces S. Naderi EF989261
100 Ca100 66 C C. aegagrus Iran Khartooran (36) 55.86 35.77 Feces S. Naderi EF989262
101 Ca101 67 C C. aegagrus Iran Khartooran (36) 55.86 35.77 Tissue S. Naderi EF989263
102 Ca102 53 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989264
103 Ca103 53 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989265
104 Ca104 53 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989266
105 Ca105 53 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989267
106 Ca106 53 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989268
107 Ca107 53 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989269
108 Ca108 54 C C. aegagrus Iran Lar, Sistan (33) 60.88 29.68 Tissue S. Naderi EF989270
109 Ca109 55 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989271
110 Ca110 54 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989272
111 Ca111 54 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Tissue S. Naderi EF989273
112 Ca112 56 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989274
113 Ca113 57 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989275
114 Ca114 57 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989276
115 Ca115 54 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989277

- 119 -
Chapter 4 Goat Domestication

116 Ca116 57 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989278
117 Ca117 57 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989279
118 Ca118 57 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989280
119 Ca119 57 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989281
120 Ca120 58 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989282
121 Ca121 59 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989283
122 Ca122 59 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989284
123 Ca123 59 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989285
124 Ca124 60 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989286
125 Ca125 41 C C. aegagrus Iran Ghorveh (18) 47.82 35.06 Feces HR. Rezaei EF989287
126 Ca126 61 C C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989288
127 Ca127 62 C C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989289
128 Ca128 63 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989290
129 Ca129 63 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989291
130 Ca130 63 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989292
131 Ca131 64 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989293
132 Ca132 64 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989294
133 Ca133 64 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989295
134 Ca134 65 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989296
135 Ca135 64 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989297
136 Ca136 64 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989298
137 Ca137 64 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989299
138 Ca138 64 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989300
139 Ca139 64 C C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989301
140 Ca140 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989302
141 Ca141 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989303
142 Ca142 57 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989304
143 Ca143 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989305
144 Ca144 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989306
145 Ca145 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989307
146 Ca146 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989308
147 Ca147 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989309

- 120 -
Chapter 4 Goat Domestication

148 Ca148 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989310
149 Ca149 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989311
150 Ca150 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989312
151 Ca151 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989313
152 Ca152 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989314
153 Ca153 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989315
154 Ca154 66 C C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989316
155 Ca155 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989317
156 Ca156 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989318
157 Ca157 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989319
158 Ca158 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989320
159 Ca159 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989321
160 Ca160 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989322
161 Ca161 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989323
162 Ca162 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989324
163 Ca163 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989325
164 Ca164 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989326
165 Ca165 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989327
166 Ca166 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989328
167 Ca167 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989329
168 Ca168 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989330
169 Ca169 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989331
170 Ca170 64 C C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989332
171 Ca171 64 C C. aegagrus Iran Khojir (21) 51.72 35.63 Feces S. Naderi EF989333
172 Ca172 67 C C. aegagrus Iran Tandooreh (39) 58.87 37.41 Tissue S. Naderi EF989334
173 Ca173 55 C C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989335
174 Ca174 68 C C. aegagrus Iran Mahneshan (17) 47.67 36.66 Feces HR. Rezaei EF989336
175 Ca175 69 C C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989337
176 Ca176 70 C C. aegagrus Turkey Erzincan (6) 39.31 39.42 Tissue A. Kence EF989338
177 Ca177 71 C C. aegagrus Turkey Gaziantep (7) 37.72 38.45 Tissue A. Kence EF989339
178 Ca178 72 C C. aegagrus Turkey Van (10) 43.22 38.29 Tissue A. Kence EF989340
179 Ca179 54 C C. aegagrus Turkey Tunceli (8) 39.34 39.07 Tissue A. Kence EF989341

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Chapter 4 Goat Domestication

180 Ca180 73 C C. aegagrus Turkey Artvin (9) 41.49 41.11 Tissue A. Kence EF989342
181 Ca181 74 C C. aegagrus Turkey Erzincan (6) 39.31 39.42 Tissue A. Kence EF989343
182 Ca182 75 C C. aegagrus Turkey Erzincan (6) 39.31 39.42 Tissue A. Kence EF989344
183 Ca183 76 C C. aegagrus Turkey Erzincan (6) 39.31 39.42 Tissue A. Kence EF989345
184 Ca184 77 C C. aegagrus Turkey Erzincan (6) 39.31 39.42 Tissue A. Kence EF989346
185 Ca185 78 C C. aegagrus Turkey Erzincan (6) 39.31 39.42 Tissue A. Kence EF989347
186 Ca186 79 C C. aegagrus Turkey Erzincan (6) 39.31 39.42 Tissue A. Kence EF989348
187 Ca187 80 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989349
188 Ca188 81 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989350
189 Ca189 44 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989351
190 Ca190 44 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989352
191 Ca191 82 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989353
192 Ca192 44 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989354
193 Ca193 44 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989355
194 Ca194 81 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989356
195 Ca195 82 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989357
196 Ca196 44 C C. aegagrus chiltanensis Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989358
197 Ca197 81 C C. aegagrus Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989359
198 Ca198 83 D C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989360
199 Ca199 84 D C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989361
200 Ca200 84 D C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989362
201 Ca201 84 D C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989363
202 Ca202 84 D C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989364
203 Ca203 84 D C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989365
204 Ca204 84 D C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989366
205 Ca205 85 D C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989367
206 Ca206 86 D C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989368
207 Ca207 87 D C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989369
208 Ca208 87 D C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989370
209 Ca209 87 D C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989371
210 Ca210 87 D C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989372
211 Ca211 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989373

- 122 -
Chapter 4 Goat Domestication

212 Ca212 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989374
213 Ca213 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989375
214 Ca214 89 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989376
215 Ca215 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989377
216 Ca216 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989378
217 Ca217 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989379
218 Ca218 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989380
219 Ca219 90 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989381
220 Ca220 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989382
221 Ca221 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989383
222 Ca222 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989384
223 Ca223 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989385
224 Ca224 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989386
225 Ca225 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989387
226 Ca226 91 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989388
227 Ca227 88 D C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989389
228 Ca228 88 D C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989390
229 Ca229 97 G C. aegagrus Iran Marakan (12) 45.24 38.85 Feces HR. Rezaei EF989391
230 Ca230 92 G C. aegagrus Iran Zalzard (13) 45.63 34.06 Feces HR. Rezaei EF989392
231 Ca231 93 G C. aegagrus Iran Zalzard (13) 45.63 34.06 Feces HR. Rezaei EF989393
232 Ca232 94 G C. aegagrus Iran Zalzard (13) 45.63 34.06 Feces HR. Rezaei EF989394
233 Ca233 92 G C. aegagrus Iran Zalzard (13) 45.63 34.06 Feces HR. Rezaei EF989395
234 Ca234 95 G C. aegagrus Iran Zalzard (13) 45.63 34.06 Feces HR. Rezaei EF989396
235 Ca235 96 G C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989397
236 Ca236 97 G C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989398
237 Ca237 97 G C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989399
238 Ca238 98 G C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989400
239 Ca239 99 C C. aegagrus Iran Dena (24) 51.32 31.06 Feces S. Naderi EF989401
240 Ca240 100 C C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989402
241 Ca241 101 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989403
242 Ca242 102 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Feces S. Naderi EF989404
243 Ca243 103 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989405

- 123 -
Chapter 4 Goat Domestication

244 Ca244 104 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989406
245 Ca245 105 C C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989407
246 Ca246 106 C C. aegagrus Iran Shoorab (32) 61.46 30.13 Feces S. Naderi EF989408
247 Ca247 107 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989409
248 Ca248 108 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989410
249 Ca249 108 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989411
250 Ca250 108 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989412
251 Ca251 109 C C. aegagrus Iran Kalmand (28) 54.79 31.28 Tissue S. Naderi EF989413
252 Ca252 110 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989414
253 Ca253 111 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989415
254 Ca254 111 C C. aegagrus Iran Khabr (31) 56.48 28.84 Feces S. Naderi EF989416
255 Ca255 112 C C. aegagrus Iran Godghool (27) 55.14 29.45 Feces S. Naderi EF989417
256 Ca256 113 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989418
257 Ca257 113 C C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989419
258 Ca258 114 C C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989420
259 Ca259 115 C C. aegagrus Iran Mehran (14) 46.12 33.31 Feces HR. Rezaei EF989421
260 Ca260 116 C C. aegagrus Iran Malayer (19) 48.95 34.21 Feces HR. Rezaei EF989422
261 Ca261 117 C C. aegagrus Iran Khartooran (36) 55.86 35.77 Feces S. Naderi EF989423
262 Ca262 118 Wild C. aegagrus Iran Mehran (14) 46.12 33.31 Tissue HR. Rezaei EF989424
263 Ca263 119 D C. aegagrus Iran Kolahghazi (23) 51.81 32.42 Feces S. Naderi EF989425
264 Ca264 120 D C. aegagrus Iran Shoorab (32) 61.46 30.13 Feces S. Naderi EF989426
265 Ca265 121 D C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989427
266 Ca266 122 D C. aegagrus Iran Golestan (37) 56.14 37.43 Feces HR. Rezaei EF989428
267 Ca267 123 D C. aegagrus Iran Malayer (19) 48.95 34.21 Feces HR. Rezaei EF989429
268 Ca268 124 D C. aegagrus Iran Mahneshan (17) 47.67 36.66 Feces HR. Rezaei EF989430
269 Ca269 125 D C. aegagrus Iran Mahneshan (17) 47.67 36.66 Feces HR. Rezaei EF989431
270 Ca270 126 D C. aegagrus Iran Bafgh (30) 56.76 31.56 Feces S. Naderi EF989432
271 Ca271 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989433
272 Ca272 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989434
273 Ca273 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989435
274 Ca274 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989436
275 Ca275 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989437

- 124 -
Chapter 4 Goat Domestication

276 Ca276 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989438
277 Ca277 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989439
278 Ca278 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989440
279 Ca279 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989441
280 Ca280 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989442
281 Ca281 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989443
282 Ca282 127 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989444
283 Ca283 128 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989445
284 Ca284 128 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989446
285 Ca285 128 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989447
286 Ca286 129 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989448
287 Ca287 130 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989449
288 Ca288 130 D C. aegagrus Iran Kavir (22) 52.19 34.71 Feces S. Naderi EF989450
289 Ca289 131 C C. aegagrus Turkey Artvin (9) 41.49 41.11 Tissue A. Kence EF989451
290 Ca290 132 Wild C. aegagrus Turkey Tunceli (8) 39.34 39.07 Bone A. Kence EF989452
291 Ca291 133 C C. aegagrus Pakistan Kirthar (43) 67.43 25.81 Feces A. T. Virk EF989453
292 Ca292 134 Wild C. aegagrus Pakistan Kirthar (43) 67.43 25.81 Feces A. T. Virk EF989454
293 Ca293 134 Wild C. aegagrus Pakistan Kirthar (43) 67.43 25.81 Feces A. T. Virk EF989455
294 Ca294 135 Wild C. aegagrus Pakistan Kirthar (43) 67.43 25.81 Feces A. T. Virk EF989456
295 Ca295 136 F C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989457
296 Ca296 136 F C. aegagrus Iran Marakan (12) 45.24 38.85 Feces HR. Rezaei EF989458
297 Ca297 136 F C. aegagrus Pakistan Kirthar (43) 67.43 25.81 Feces A. T. Virk EF989459
298 Ca298 136 F C. aegagrus Turkey Erzincan (6) 39.31 39.42 Tissue A. Kence EF989460
299 Ca299 136 F C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue P. Weinberg EF989461
300 Ca300 137 F C. aegagrus Turkey Akseki (3) 31.47 37.21 Feces A. Kence EF989462
301 Ca301 137 F C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989463
302 Ca302 137 F C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989464
303 Ca303 137 F C. aegagrus Turkey Akseki (3) 31.47 37.21 Feces A. Kence EF989465
304 Ca304 138 F C. aegagrus Azerbaijan Nakhitchevan (15) 45.26 39.25 Feces P. Weinberg EF989466
305 Ca305 139 F C. aegagrus Turkey Van (10) 43.22 38.29 Tissue A. Kence EF989467
306 Ca306 140 F C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989468
307 Ca307 141 F C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue P. Weinberg EF989469

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Chapter 4 Goat Domestication

308 Ca308 142 F C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989470
309 Ca309 143 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989471
310 Ca310 144 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989472
311 Ca311 145 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989473
312 Ca312 145 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989474
313 Ca313 145 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989475
314 Ca314 145 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989476
315 Ca315 145 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989477
316 Ca316 145 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989478
317 Ca317 145 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989479
318 Ca318 145 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989480
319 Ca319 145 Wild C. aegagrus Turkey Finike (1) 30.8 36.17 Feces A. Kence EF989481
320 Ca320 146 Wild C. aegagrus Iran Khartooran (36) 55.86 35.77 Feces S. Naderi EF989482
321 Ca321 147 Wild C. aegagrus Iran Khartooran (36) 55.86 35.77 Feces S. Naderi EF989483
322 Ca322 147 Wild C. aegagrus Iran Khartooran (36) 55.86 35.77 Feces S. Naderi EF989484
323 Ca323 148 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Feces A. Kence EF989485
324 Ca324 149 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Feces A. Kence EF989486
325 Ca325 149 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Tissue A. Kence EF989487
326 Ca326 149 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Tissue A. Kence EF989488
327 Ca327 150 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Tissue A. Kence EF989489
328 Ca328 151 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Tissue A. Kence EF989490
329 Ca329 152 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Feces A. Kence EF989491
330 Ca330 153 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Tissue A. Kence EF989492
331 Ca331 154 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989493
332 Ca332 154 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Tissue A. Kence EF989494
333 Ca333 155 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Tissue A. Kence EF989495
334 Ca334 156 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Tissue A. Kence EF989496
335 Ca335 157 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989497
336 Ca336 158 Wild C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue P. Weinberg EF989498
337 Ca337 159 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989499
338 Ca338 159 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989500
339 Ca339 160 Wild C. aegagrus Iran Khoshyeylagh (35) 55.43 36.71 Feces S. Naderi EF989501

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Chapter 4 Goat Domestication

340 Ca340 161 Wild C. aegagrus Iran Golestan (37) 56.14 37.43 Tissue S. Naderi EF989502
341 Ca341 162 Wild C. aegagrus Iran Golestan (37) 56.14 37.43 Feces S. Naderi EF989503
342 Ca342 163 Wild C. aegagrus Iran Khojir (21) 51.72 35.63 Feces S. Naderi EF989504
343 Ca343 163 Wild C. aegagrus Iran Khojir (21) 51.72 35.63 Feces S. Naderi EF989505
344 Ca344 164 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989506
345 Ca345 164 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989507
346 Ca346 165 Wild C. aegagrus Iran Golestan (37) 56.14 37.43 Feces S. Naderi EF989508
347 Ca347 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989509
348 Ca348 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989510
349 Ca349 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989511
350 Ca350 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989512
351 Ca351 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989513
352 Ca352 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989514
353 Ca353 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989515
354 Ca354 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989516
355 Ca355 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989517
356 Ca356 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989518
357 Ca357 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989519
358 Ca358 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989520
359 Ca359 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989521
360 Ca360 166 Wild C. aegagrus Iran Salook (38) 57.26 37.22 Feces S. Naderi EF989522
361 Ca361 167 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989523
362 Ca362 167 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989524
363 Ca363 168 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989525
364 Ca364 168 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989526
365 Ca365 169 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989527
366 Ca366 169 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989528
367 Ca367 169 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989529
368 Ca368 169 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989530
369 Ca369 169 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989531
370 Ca370 170 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989532
371 Ca371 171 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989533

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Chapter 4 Goat Domestication

372 Ca372 171 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989534
373 Ca373 171 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989535
374 Ca374 171 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989536
375 Ca375 171 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989537
376 Ca376 171 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989538
377 Ca377 171 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989539
378 Ca378 171 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989540
379 Ca379 171 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Tissue S. Naderi EF989541
380 Ca380 172 Wild C. aegagrus Iran Parvar (34) 53.51 35.97 Feces S. Naderi EF989542
381 Ca381 173 Wild C. aegagrus Iran Khartooran (36) 55.86 35.77 Tissue S. Naderi EF989543
382 Ca382 174 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989544
383 Ca383 174 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989545
384 Ca384 174 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Feces S. Naderi EF989546
385 Ca385 174 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Tissue S. Naderi EF989547
386 Ca386 174 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Tissue S. Naderi EF989548
387 Ca387 174 Wild C. aegagrus Iran Tandooreh (39) 58.87 37.41 Tissue S. Naderi EF989549
388 Ca388 175 Wild C. aegagrus Iran Khartooran (36) 55.86 35.77 Feces S. Naderi EF989550
389 Ca389 175 Wild C. aegagrus Turkey Akseki (3) 31.47 37.21 Feces A. Kence EF989551
390 Ca390 176 Wild C. aegagrus Iran Marakan (12) 45.24 38.85 Feces HR. Rezaei EF989552
391 Ca391 177 Wild C. aegagrus Azerbaijan Nakhitchevan (15) 45.26 39.25 Tissue P. Weinberg EF989553
392 Ca392 177 Wild C. aegagrus Turkey Soyuk (5) 35.17 41.51 Tissue A. Kence EF989554
393 Ca393 178 Wild C. aegagrus Turkey Soyuk (5) 35.17 41.51 Tissue A. Kence EF989555
394 Ca394 179 Wild C. aegagrus Iran Marakan (12) 45.24 38.85 Feces HR. Rezaei EF989556
395 Ca395 180 Wild C. aegagrus Iran Marakan (12) 45.24 38.85 Feces HR. Rezaei EF989557
396 Ca396 180 Wild C. aegagrus Iran Marakan (12) 45.24 38.85 Feces HR. Rezaei EF989558
397 Ca397 181 Wild C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue A. Kence EF989559
398 Ca398 182 Wild C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue P. Weinberg EF989560
399 Ca399 183 Wild C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue P. Weinberg EF989561
400 Ca400 184 Wild C. aegagrus Turkey Van (10) 43.22 38.29 Tissue A. Kence EF989562
401 Ca401 185 Wild C. aegagrus Iran Dahaj (29) 54.87 30.57 Feces S. Naderi EF989563
402 Ca402 186 Wild C. aegagrus Iran Malayer (19) 48.95 34.21 Tissue HR. Rezaei EF989564
403 Ca403 186 Wild C. aegagrus Iran Malayer (19) 48.95 34.21 Tissue HR. Rezaei EF989565

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Chapter 4 Goat Domestication

404 Ca404 187 Wild C. aegagrus Iran Malayer (19) 48.95 34.21 Feces HR. Rezaei EF989566
405 Ca405 188 Wild C. aegagrus Iran Malayer (19) 48.95 34.21 Feces HR. Rezaei EF989567
406 Ca406 189 Wild C. aegagrus Iran Malayer (19) 48.95 34.21 Feces HR. Rezaei EF989568
407 Ca407 190 Wild C. aegagrus Pakistan Hazarganji (41) 66.11 27.28 Horn A. T. Virk EF989569
408 Ca408 191 Wild C. aegagrus Iran Mehran (14) 46.12 33.31 Feces HR. Rezaei EF989570
409 Ca409 192 Wild C. aegagrus Iran Mehran (14) 46.12 33.31 Tissue HR. Rezaei EF989571
410 Ca410 193 Wild C. aegagrus Iran Mehran (14) 46.12 33.31 Feces HR. Rezaei EF989572
411 Ca411 194 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989573
412 Ca412 195 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989574
413 Ca413 196 Wild C. aegagrus Turkey Tunceli (8) 39.34 39.07 Tissue A. Kence EF989575
414 Ca414 197 Wild C. aegagrus Turkey Tunceli (8) 39.34 39.07 Tissue A. Kence EF989576
415 Ca415 198 Wild C. aegagrus Iran Mehran (14) 46.12 33.31 Tissue HR. Rezaei EF989577
416 Ca416 199 Wild C. aegagrus Iran Malayer (19) 48.95 34.21 Tissue HR. Rezaei EF989578
417 Ca417 200 Wild C. aegagrus Turkey Soyuk (5) 35.17 41.51 Horn A. Kence EF989579
418 Ca418 201 Wild C. aegagrus Turkey Soyuk (5) 35.17 41.51 Horn A. Kence EF989580
419 Ca419 201 Wild C. aegagrus Turkey Soyuk (5) 35.17 41.51 Horn A. Kence EF989581
420 Ca420 201 Wild C. aegagrus Turkey Soyuk (5) 35.17 41.51 Tissue A. Kence EF989582
421 Ca421 201 Wild C. aegagrus Azerbaijan Nakhitchevan (15) 45.26 39.25 Tissue P. Weinberg EF989583
422 Ca422 201 Wild C. aegagrus Azerbaijan Nakhitchevan (15) 45.26 39.25 Feces P. Weinberg EF989584
423 Ca423 201 Wild C. aegagrus Azerbaijan Nakhitchevan (15) 45.26 39.25 Feces P. Weinberg EF989585
424 Ca424 202 Wild C. aegagrus Iran Golestan (37) 56.14 37.43 Tissue HR. Rezaei EF989586
425 Ca425 203 Wild C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989587
426 Ca426 204 Wild C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989588
427 Ca427 205 Wild C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989589
428 Ca428 206 Wild C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989590
429 Ca429 207 Wild C. aegagrus Iran Mahneshan (17) 47.67 36.66 Feces HR. Rezaei EF989591
430 Ca430 208 Wild C. aegagrus Iran Mahneshan (17) 47.67 36.66 Feces HR. Rezaei EF989592
431 Ca431 209 Wild C. aegagrus Turkey Tunceli (8) 39.34 39.07 Tissue A. Kence EF989593
432 Ca432 210 Wild C. aegagrus Turkey Tunceli (8) 39.34 39.07 Tissue A. Kence EF989594
433 Ca433 211 Wild C. aegagrus Turkey Tunceli (8) 39.34 39.07 Tissue A. Kence EF989595
434 Ca434 212 Wild C. aegagrus Iran Mahneshan (17) 47.67 36.66 Feces HR. Rezaei EF989596
435 Ca435 213 Wild C. aegagrus Iran Khojir (21) 51.72 35.63 Feces S. Naderi EF989597

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Chapter 4 Goat Domestication

436 Ca436 214 Wild C. aegagrus Iran Khojir (21) 51.72 35.63 Feces S. Naderi EF989598
437 Ca437 215 Wild C. aegagrus Iran Khojir (21) 51.72 35.63 Feces S. Naderi EF989599
438 Ca438 216 Wild C. aegagrus Iran Khojir (21) 51.72 35.63 Feces S. Naderi EF989600
439 Ca439 217 Wild C. aegagrus Iran Khojir (21) 51.72 35.63 Feces S. Naderi EF989601
440 Ca440 218 Wild C. aegagrus Iran Khojir (21) 51.72 35.63 Feces S. Naderi EF989602
441 Ca441 219 Wild C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989603
442 Ca442 220 Wild C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989604
443 Ca443 221 Wild C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989605
444 Ca444 222 Wild C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989606
445 Ca445 223 Wild C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989607
446 Ca446 224 Wild C. aegagrus Iran Bamoo (26) 52.68 29.69 Feces S. Naderi EF989608
447 Ca447 225 Wild C. aegagrus Iran Khartooran (36) 55.86 35.77 Feces S. Naderi EF989609
448 Ca448 226 Wild C. aegagrus Iran Khartooran (36) 55.86 35.77 Feces S. Naderi EF989610
449 Ca449 227 Wild C. aegagrus Iran Mahneshan (17) 47.67 36.66 Feces HR. Rezaei EF989611
450 Ca450 228 Wild C. aegagrus Iran Marakan (12) 45.24 38.85 Feces HR. Rezaei EF989612
451 Ca451 229 Wild C. aegagrus Iran Ghazvin (20) 49.57 36.09 Tissue HR. Rezaei EF989613
452 Ca452 230 Wild C. aegagrus Iran Zalzard (13) 45.63 34.06 Feces HR. Rezaei EF989614
453 Ca453 231 C C. aegagrus Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989615
454 Ca454 232 C C. aegagrus Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989616
455 Ca455 233 D C. aegagrus Turkey Akseki (3) 31.47 37.21 Tissue A. Kence EF989617
456 Ca456 234 C C. aegagrus Turkey Mersin (4) 34.36 36.21 Tissue A. Kence EF989618
457 Ca457 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989619
458 Ca458 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989620
459 Ca459 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989621
460 Ca460 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989622
461 Ca461 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989623
462 Ca462 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989624
463 Ca463 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989625
464 Ca464 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989626
465 Ca465 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989627
466 Ca466 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989628
467 Ca467 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989629

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Chapter 4 Goat Domestication

468 Ca468 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989630
469 Ca469 235 Wild C. aegagrus Turkey Mersin (4) 34.36 36.21 Feces A. Kence EF989631
470 Ca470 236 Wild C. aegagrus Turkey Van (10) 43.22 38.29 Tissue A. Kence EF989632
471 Ca471 236 Wild C. aegagrus Azerbaijan Nakhitchevan (15) 45.26 39.25 Tissue P. Weinberg EF989633
472 Ca472 237 Wild C. aegagrus Pakistan Hazarganji (41) 66.11 27.28 Feces A. T. Virk EF989634
473 Ca473 238 Wild C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue P. Weinberg EF989635
474 Ca474 239 Wild C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue P. Weinberg EF989636
475 Ca475 240 Wild C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue P. Weinberg EF989637
476 Ca476 241 Wild C. aegagrus Dagestan AudiKoisu (16) 46.71 43.25 Tissue P. Weinberg EF989638
477 Ca477 242 Wild C. aegagrus Pakistan Kirthar (43) 67.43 25.81 Feces A. T. Virk EF989639
478 Ca478 243 Wild C. aegagrus Pakistan Kirthar (43) 67.43 25.81 Feces A. T. Virk EF989640
479 Ca479 244 Wild C. aegagrus Pakistan Kirthar (43) 67.43 25.81 Feces A. T. Virk EF989641
480 Ca480 245 Wild C. aegagrus Pakistan Kirthar (43) 67.43 25.81 Feces A. T. Virk EF989642
481 Ca481 246 Wild C. aegagrus Pakistan Dureji (42) 67.43 25.81 Tissue A. T. Virk EF989643
482 Ca482 247 Wild C. aegagrus Pakistan Dureji (42) 67.43 25.81 Tissue A. T. Virk EF989644
483 Ca483 248 F C. aegagrus Turkey Van (10) 43.22 38.29 Tissue A. Kence EF989645
484 Ca484 249 Wild C. aegagrus Turkmenistan Turkmenistan (40) 65.49 38.37 Tissue G. Luikart AJ317866
485 Ca485 250 Wild C. aegagrus Turkmenistan Turkmenistan (40) 65.49 38.37 Tissue G. Luikart AJ317867
486 Ca486 251 Wild C. aegagrus blythi Pakistan Kirthar (43) 67.43 25.81 Tissue Sultana AB110590
487 Ca487 251 Wild C. aegagrus blythi Pakistan Kirthar (43) 67.43 25.81 Tissue Sultana AB110591

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 Chapter 4 Goat Domestication

Supplementary Table 4.2. Geographic origin and characteristics of the domestic and wild goat samples used for AFLP study.

(Abbreviations used for the different breeds: CAE, C. aegagrus; VAL, Valdostana; BIO, Bionda dell'Adamello; CAM, Camosclata; RAI, Raini;

LOC, Iranian local breeds; KUR, Kurdi; KSH, Kermanshah; SAN, Sanandaj).

NO. Code Species Country Population (Breed) Longitude(E) Latitude(N) Sample Type Collector
1 ChIr01 C. hircus IRAN Bashgol Ghazvin (LOC) 49.56 36.12 Tissue HR. Rezaei
2 ChIr02 C. hircus IRAN Bashgol Ghazvin (LOC) 49.56 36.12 Tissue HR. Rezaei
3 ChIr03 C. hircus IRAN Bashgol Ghazvin (LOC) 49.56 36.12 Tissue HR. Rezaei
4 ChIr04 C. hircus IRAN Bashgol Ghazvin (LOC) 49.56 36.12 Tissue HR. Rezaei
5 ChIr05 C. hircus IRAN Bashgol Ghazvin (LOC) 49.56 36.12 Tissue HR. Rezaei
6 ChIr06 C. hircus IRAN Bashgol Ghazvin (LOC) 49.56 36.12 Tissue HR. Rezaei
7 ChIr07 C. hircus IRAN Bashgol Ghazvin (LOC) 49.56 36.12 Tissue HR. Rezaei
8 ChIr08 C. hircus IRAN Alamout Gazvin (LOC) 49.57 36.11 Tissue HR. Rezaei
9 ChIr09 C. hircus IRAN Alamout Gazvin (LOC) 49.57 36.11 Tissue HR. Rezaei
10 ChIr10 C. hircus IRAN Alamout Gazvin (LOC) 49.57 36.11 Tissue HR. Rezaei
11 ChIr11 C. hircus IRAN Alamout Gazvin (LOC) 49.57 36.11 Tissue HR. Rezaei
12 ChIr12 C. hircus IRAN Angouran Zanjan – Mahneshan (LOC) 47.67 36.67 Tissue HR. Rezaei
13 ChIr13 C. hircus IRAN Marakan, Western Azarbaijan (LOC) 45.24 38.84 Tissue HR. Rezaei
14 ChIr14 C. hircus IRAN Marakan, Western Azarbaijan (LOC) 45.24 38.84 Tissue HR. Rezaei
15 ChIr15 C. hircus IRAN Marakan, Western Azarbaijan (LOC) 45.24 38.84 Tissue HR. Rezaei
16 ChIr16 C. hircus IRAN Marakan, Western Azarbaijan (LOC) 45.24 38.84 Tissue HR. Rezaei
17 ChIr17 C. hircus IRAN Ghorveh Sanandadj (LOC) 47.82 35.06 Tissue HR. Rezaei
18 ChIr18 C. hircus IRAN Ghorveh Sanandadj (LOC) 47.82 35.06 Tissue HR. Rezaei
19 ChIr19 C. hircus IRAN Mehran (LOC) 46.11 33.31 Tissue HR. Rezaei
20 ChIr20 C. hircus IRAN Mehran (LOC) 46.11 33.31 Tissue HR. Rezaei

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Chapter 4 Goat Domestication

21 ChIr21 C. hircus IRAN Dareh Shahr Ilam (LOC) 47.38 33.19 Tissue HR. Rezaei
22 ChIr22 C. hircus IRAN Dareh Shahr Ilam (LOC) 47.38 33.19 Tissue HR. Rezaei
23 ChIr23 C. hircus IRAN Khoram- Abad (LOC) 48.16 33.58 Tissue HR. Rezaei
24 ChIr24 C. hircus IRAN Azna (LOC) 49.35 33.44 Tissue HR. Rezaei
25 ChIr25 C. hircus IRAN Azna (LOC) 49.35 33.44 Tissue HR. Rezaei
26 ChIr26 C. hircus IRAN Azna (LOC) 49.35 33.44 Tissue HR. Rezaei
27 ChIr27 C. hircus IRAN Parvar (LOC) 55.51 36.01 Tissue S. Naderi
28 ChIr28 C. hircus IRAN Parvar (LOC) 55.51 36.01 Tissue S. Naderi
29 ChIr29 C. hircus IRAN Khosh Yeylagh, Dasht_e_Zardabeh (LOC) 55.47 34.75 Tissue S. Naderi
30 ChIr30 C. hircus IRAN Khosh Yeylagh, Dasht_e_Zardabeh (LOC) 55.47 34.75 Tissue S. Naderi
31 ChIr31 C. hircus IRAN Khosh Yeylagh, Dasht_e_Zardabeh (LOC) 55.47 34.75 Tissue S. Naderi
32 ChIr32 C. hircus IRAN Khartooran (LOC) 55.86 35.79 Tissue S. Naderi
33 ChIr33 C. hircus IRAN Khartooran (LOC) 55.86 35.79 Tissue S. Naderi
34 ChIr34 C. hircus IRAN Nosratabad Systan & Baloochestan (LOC) 59.87 29.97 Tissue S. Naderi
35 ChIr35 C. hircus IRAN Ghamishloo (LOC) 51.22 32.85 Tissue S. Naderi
36 ChIr36 C. hircus IRAN Ghamishloo (LOC) 51.22 32.85 Tissue S. Naderi
37 ChIr37 C. hircus IRAN Ghamishloo (LOC) 51.22 32.85 Tissue S. Naderi
38 ChIr38 C. hircus IRAN Ghamishloo (LOC) 51.22 32.85 Tissue S. Naderi
39 ChIr39 C. hircus IRAN Kooh-e-Bafgh (LOC) 55.67 31.85 Tissue S. Naderi
40 ChIr40 C. hircus IRAN Kooh-e-Bafgh (LOC) 55.67 31.85 Tissue S. Naderi
41 ChIr41 C. hircus IRAN Kooh-e-Bafgh (LOC) 55.67 31.85 Tissue S. Naderi
42 ChIr42 C. hircus IRAN Kooh-e-Bafgh (LOC) 55.67 31.85 Tissue S. Naderi
43 ChIr43 C. hircus IRAN Kooh-e-Bafgh (LOC) 55.67 31.85 Tissue S. Naderi
44 ChIr44 C. hircus IRAN Khabr National Park (LOC) 56.48 28.84 Tissue S. Naderi
45 ChIr45 C. hircus IRAN Khabr National Park (LOC) 56.48 28.84 Tissue S. Naderi
46 ChIr46 C. hircus IRAN Khabr National Park (LOC) 56.48 28.84 Tissue S. Naderi
47 ChIr47 C. hircus IRAN Khabr National Park (LOC) 56.48 28.84 Tissue S. Naderi
48 ChIr48 C. hircus IRAN Khabr National Park (LOC) 56.48 28.84 Tissue S. Naderi

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49 ChIr49 C. hircus IRAN Khabr National Park (LOC) 56.48 28.84 Tissue S. Naderi
50 ChIr50 C. hircus IRAN Khabr National Park (LOC) 56.48 28.84 Tissue S. Naderi
51 ChIr51 C. hircus IRAN God-e-Ghool Restricted Area (LOC) 55.14 29.45 Tissue S. Naderi
52 ChIr52 C. hircus IRAN God-e-Ghool Restricted Area (LOC) 55.14 29.45 Tissue S. Naderi
53 ChIr53 C. hircus IRAN God-e-Ghool Restricted Area (LOC) 55.14 29.45 Tissue S. Naderi
54 ChIr54 C. hircus IRAN God-e-Ghool Restricted Area (LOC) 55.14 29.45 Tissue S. Naderi
55 ChIr55 C. hircus IRAN God-e-Ghool Restricted Area (LOC) 55.14 29.45 Tissue S. Naderi
56 ChIr56 C. hircus IRAN God-e-Ghool Restricted Area (LOC) 55.14 29.45 Tissue S. Naderi
57 ChIr57 C. hircus IRAN God-e-Ghool Restricted Area (LOC) 55.14 29.45 Tissue S. Naderi
58 ChIr58 C. hircus IRAN Dahaj Shahr Babak (LOC) 54.87 30.57 Tissue S. Naderi
59 ChIr59 C. hircus IRAN Dahaj Shahr Babak (LOC) 54.87 30.57 Tissue S. Naderi
60 ChIr60 C. hircus IRAN Dahaj Shahr Babak (LOC) 54.87 30.57 Tissue S. Naderi
61 ChIr61 C. hircus IRAN Dahaj Shahr Babak (LOC) 54.87 30.57 Tissue S. Naderi
62 ChIr62 C. hircus IRAN Basiran (LOC) 52.85 30.88 Tissue S. Naderi
63 ChIr63 C. hircus IRAN Basiran (LOC) 52.85 30.88 Tissue S. Naderi
64 ChIr64 C. hircus IRAN Basiran (LOC) 52.85 30.88 Tissue S. Naderi
65 ChIr65 C. hircus IRAN Basiran (LOC) 52.85 30.88 Tissue S. Naderi
66 ChIr66 C. hircus IRAN Basiran (LOC) 52.85 30.88 Tissue S. Naderi
67 ChIr67 C. hircus IRAN Basiran (LOC) 52.85 30.88 Tissue S. Naderi
68 ChIr68 C. hircus IRAN Basiran (LOC) 52.85 30.88 Tissue S. Naderi
69 ChIr69 C. hircus IRAN Zaraab, Around Baft City in Kerman Province (RAI) 56.61 29.23 Tissue A. Rafat
70 ChIr70 C. hircus IRAN Zaraab, Around Baft City in Kerman Province (RAI) 56.61 29.23 Tissue A. Rafat
71 ChIr71 C. hircus IRAN Absaalaan-sad, Around Baft City in Kerman Province (RAI) 56.61 29.24 Tissue A. Rafat
72 ChIr72 C. hircus IRAN Absaalaan-sad, Around Baft City in Kerman Province (RAI) 56.61 29.24 Tissue A. Rafat
73 ChIr73 C. hircus IRAN Zaraab, Around Baft City in Kerman Province (RAI) 56.61 29.23 Tissue A. Rafat
74 ChIr74 C. hircus IRAN Zaraab, Around Baft City in Kerman Province (RAI) 56.61 29.23 Tissue A. Rafat
75 ChIr75 C. hircus IRAN Khabr, Around Baft City in Kerman Province (RAI) 56.82 29.41 Tissue A. Rafat
76 ChIr76 C. hircus IRAN Jangal-cha, Around Baft City in Kerman Province (RAI) 56.37 29.93 Tissue A. Rafat

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77 ChIr77 C. hircus IRAN Jangal-cha, Around Baft City in Kerman Province (RAI) 56.37 29.93 Tissue A. Rafat
78 ChIr78 C. hircus IRAN Ghaasemi, Around Baft City in Kerman Province (RAI) 56.81 29.65 Tissue A. Rafat
79 ChIr79 C. hircus IRAN Ghaasemi, Around Baft City in Kerman Province (RAI) 56.81 29.65 Tissue A. Rafat
80 ChIr80 C. hircus IRAN Gorguye, Around Baft City in Kerman Province (RAI) 56.21 29.23 Tissue A. Rafat
81 ChIr81 C. hircus IRAN Gorguye, Around Baft City in Kerman Province(RAI) 56.21 29.23 Tissue A. Rafat
82 ChIr82 C. hircus IRAN Zaraab, Around Baft City in Kerman Province (RAI) 56.6 29.23 Tissue A. Rafat
83 ChIr83 C. hircus IRAN Zaraab, Around Baft City in Kerman Province (RAI) 56.6 29.23 Tissue A. Rafat
84 ChIr84 C. hircus IRAN Baft (RAI) 56.6 29.44 Tissue A. Rafat
85 ChIr85 C. hircus IRAN Baft (RAI) 56.6 29.44 Tissue A. Rafat
86 ChIr86 C. hircus IRAN Baft (RAI) 56.6 29.44 Tissue A. Rafat
87 ChIr87 C. hircus IRAN Baft (RAI) 56.6 29.44 Tissue A. Rafat
88 ChIr88 C. hircus IRAN Baft-Hoseinabad, Around Baft City in Kerman Province (RAI) 56.26 29.23 Tissue A. Rafat
89 ChIr89 C. hircus IRAN Baft-Hoseinabad, Around Baft City in Kerman Province (RAI) 56.26 29.23 Tissue A. Rafat
90 ChIr90 C. hircus IRAN Baft, Jamalabad, Around Baft City in Kerman Province (RAI) 56.32 29.73 Tissue A. Rafat
91 ChIr91 C. hircus IRAN Baft, Jamalabad, Around Baft City in Kerman Province (RAI) 56.32 29.73 Tissue A. Rafat
92 ChIr92 C. hircus IRAN Chalekuye, Around Baft City in Kerman Province (RAI) 56.91 29.87 Tissue A. Rafat
93 ChIr93 C. hircus IRAN Chalekuye, Around Baft City in Kerman Province (RAI) 56.91 29.87 Tissue A. Rafat
94 ChIr94 C. hircus IRAN Baft-mahdabad, Around Baft City in Kerman Province (RAI) 56.05 29.32 Tissue A. Rafat
95 ChIr95 C. hircus IRAN Baft-mahdabad, Around Baft City in Kerman Province (RAI) 56.05 29.32 Tissue A. Rafat
96 ChIr96 C. hircus IRAN Baft-dughan, Around Baft City in Kerman Province (RAI) 56.58 29.32 Tissue A. Rafat
97 ChIr97 C. hircus IRAN Baft-dughan, Around Baft City in Kerman Province (RAI) 56.58 29.32 Tissue A. Rafat
98 ChIr98 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
99 ChIr99 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
100 ChIr100 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
101 ChIr101 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
102 ChIr102 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
103 ChIr103 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
104 ChIr104 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat

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105 ChIr105 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
106 ChIr106 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
107 ChIr107 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
108 ChIr108 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
109 ChIr109 C. hircus IRAN Armarde-DashtBozorg, Around Baneh city (KUR) 46.28 36.55 Tissue A. Rafat
110 ChIr110 C. hircus IRAN Armarde-DashtBozorg, Around Baneh city (KUR) 46.28 36.55 Tissue A. Rafat
111 ChIr111 C. hircus IRAN Armarde-DashtBozorg, Around Baneh city (KUR) 46.28 36.55 Tissue A. Rafat
112 ChIr112 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
113 ChIr113 C. hircus IRAN Torjan (KUR) 46.17 36.55 Tissue A. Rafat
114 ChIr114 C. hircus IRAN Armarde-DashtBozorg, Around Baneh city (KUR) 46.28 36.55 Tissue A. Rafat
115 ChIr115 C. hircus IRAN Armarde-DashtBozorg, Around Baneh city (KUR) 46.28 36.55 Tissue A. Rafat
116 ChIr116 C. hircus IRAN Armarde-DashtBozorg, Around Baneh city (KUR) 46.28 36.55 Tissue A. Rafat
117 ChIr117 C. hircus IRAN Armarde-DashtBozorg, Around Baneh city (KUR) 46.28 36.55 Tissue A. Rafat
118 ChIr118 C. hircus IRAN Saqqez (KUR) 46.29 36.13 Tissue A. Rafat
119 ChIr119 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
120 ChIr120 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
121 ChIr121 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
122 ChIr122 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
123 ChIr123 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
124 ChIr124 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
125 ChIr125 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
126 ChIr126 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
127 ChIr127 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
128 ChIr128 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
129 ChIr129 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
130 ChIr130 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
131 ChIr131 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
132 ChIr132 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash

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Chapter 4 Goat Domestication

133 ChIr133 C. hircus IRAN Kurdistan-Kermanshah (KSH) 46.73 34.25 Tissue HR. Naghash
134 ChIr134 C. hircus IRAN Kurdistan-Sanandaj (SAN) 46.85 35.45 Tissue HR. Naghash
135 ChIr135 C. hircus IRAN Kurdistan-Sanandaj (SAN) 46.85 35.45 Tissue HR. Naghash
136 ChIr136 C. hircus IRAN Kurdistan-Sanandaj (SAN) 46.85 35.45 Tissue HR. Naghash
137 ChIr137 C. hircus IRAN Kurdistan-Sanandaj (SAN) 46.85 35.45 Tissue HR. Naghash
138 ChIr138 C. hircus IRAN Kurdistan-Sanandaj (SAN) 46.85 35.45 Tissue HR. Naghash
139 ChIr139 C. hircus IRAN Kurdistan-Sanandaj (SAN) 46.85 35.45 Tissue HR. Naghash
140 ChIr140 C. hircus IRAN Kurdistan-Sanandaj (SAN) 46.85 35.45 Tissue HR. Naghash
141 ChIr141 C. hircus IRAN Kurdistan-Sanandaj (SAN) 46.85 35.45 Tissue HR. Naghash
142 ChIr142 C. hircus IRAN Kurdistan-Sanandaj (SAN) 46.85 35.45 Tissue HR. Naghash
143 CaIRI01 C. aegagrus IRAN Khartooran Protected Area (CAE) 55.86 35.77 Tissue S. Naderi
144 CaIRI04 C. aegagrus IRAN Gazvin (CAE) 49.57 36.09 Tissue HR. Rezaei
145 CaIRI05 C. aegagrus IRAN Gazvin (CAE) 49.57 36.09 Tissue HR. Rezaei
146 CaIRI06 C. aegagrus IRAN Lashkar-Dar Malayer (CAE) 48.95 34.21 Tissue HR. Rezaei
147 CaIRI08 C. aegagrus IRAN Mehran (CAE) 46.12 33.31 Tissue HR. Rezaei
148 CaIRI11 C. aegagrus IRAN Tandooreh National Park (CAE) 58.87 37.41 Tissue S. Naderi
149 CaIRI12 C. aegagrus IRAN Tandooreh National Park (CAE) 58.87 37.41 Tissue S. Naderi
150 CaIRI14 C. aegagrus IRAN Gazvin (CAE) 49.57 36.09 Tissue HR. Rezaei
151 CaIRI15 C. aegagrus IRAN Gazvin (CAE) 49.57 36.09 Tissue HR. Rezaei
152 CaIRI17 C. aegagrus IRAN Golestan National Park (CAE) 56.14 37.43 Tissue HR. Rezaei
153 CaIRI19 C. aegagrus IRAN Gazvin (CAE) 49.57 36.09 Tissue HR. Rezaei
154 CaIRI20 C. aegagrus IRAN Gazvin (CAE) 49.57 36.09 Tissue HR. Rezaei
155 CaIRI26 C. aegagrus IRAN Kalmand-Bahadoran Protected Area (CAE) 54.79 31.28 Tissue S. Naderi
156 CaIRI28 C. aegagrus IRAN Gazvin (CAE) 49.57 36.09 Tissue HR. Rezaei
157 CaIRI33 C. aegagrus IRAN Gazvin (CAE) 49.57 36.09 Tissue HR. Rezaei
158 CaIRI35 C. aegagrus IRAN Mehran (CAE) 46.12 33.31 Tissue HR. Rezaei
159 CaIRI36 C. aegagrus IRAN Lashkar-Dar Malayer (CAE) 48.95 34.21 Tissue HR. Rezaei
160 CaIRI39 C. aegagrus IRAN Bavanat Restricted Area (CAE) 53.91 30.31 Tissue S. Naderi
161 CaIRI40 C. aegagrus IRAN Bavanat Restricted Area (CAE) 53.91 30.31 Tissue S. Naderi
162 ChItCAM01 C. hircus ITALY Boario_Brescia_Lombardy (CAM) 10.1465 45.8846 Whole blood S. Giovenzana
163 ChItCAM02 C. hircus ITALY Boario_Brescia_Lombardy (CAM) 10.1465 45.8846 Whole blood S. Giovenzana

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164 ChItCAM03 C. hircus ITALY Boario_Brescia_Lombardy (CAM) 10.1465 45.8846 Whole blood S. Giovenzana
165 ChItCAM04 C. hircus ITALY Boario_Brescia_Lombardy (CAM) 10.1439 45.8961 Whole blood S. Giovenzana
166 ChItCAM05 C. hircus ITALY Boario_Brescia_Lombardy (CAM) 10.1439 45.8961 Whole blood S. Giovenzana
167 ChItCAM06 C. hircus ITALY Boario_Brescia_Lombardy (CAM) 10.1439 45.8961 Whole blood S. Giovenzana
168 ChItCAM07 C. hircus ITALY Boario_Brescia_Lombardy (CAM) 10.2311 45.9297 Whole blood S. Giovenzana
169 ChItCAM08 C. hircus ITALY Boario_Brescia_Lombardy (CAM) 10.2311 45.9297 Whole blood S. Giovenzana
170 ChItCAM10 C. hircus ITALY Boario_Brescia_Lombardy (CAM) 10.2311 45.9297 Whole blood S. Giovenzana
171 ChItCAM11 C. hircus ITALY Prestine_Brescia_Lombardy (CAM) 10.321 45.9229 Whole blood S. Giovenzana
172 ChItCAM12 C. hircus ITALY Prestine_Brescia_Lombardy (CAM) 10.321 45.9229 Whole blood S. Giovenzana
173 ChItCAM14 C. hircus ITALY Prestine_Brescia_Lombardy (CAM) 10.321 45.9229 Whole blood S. Giovenzana
174 ChItCAM16 C. hircus ITALY Pincamuno_Brescia_Lombardy (CAM) 10.3212 45.9343 Whole blood S. Giovenzana
175 ChItCAM17 C. hircus ITALY Pincamuno_Brescia_Lombardy (CAM) 10.3212 45.9343 Whole blood S. Giovenzana
176 ChItCAM18 C. hircus ITALY Pincamuno_Brescia_Lombardy (CAM) 10.3212 45.9343 Whole blood S. Giovenzana
177 ChItCAM19 C. hircus ITALY Piantedo_Sondrio_Lombardy (CAM) 9.4389 46.1408 Whole blood S. Giovenzana
178 ChItCAM20 C. hircus ITALY Piantedo_Sondrio_Lombardy (CAM) 9.4389 46.1408 Whole blood S. Giovenzana
179 ChItCAM21 C. hircus ITALY Piantedo_Sondrio_Lombardy (CAM) 9.4389 46.1408 Whole blood S. Giovenzana
180 ChItCAM22 C. hircus ITALY San pellegrino terme_Bergamo_Lombardy (CAM) 9.6384 45.869 Whole blood S. Giovenzana
181 ChItCAM23 C. hircus ITALY San pellegrino terme_Bergamo_Lombardy (CAM) 9.6384 45.869 Whole blood S. Giovenzana
182 ChItCAM24 C. hircus ITALY San pellegrino terme_Bergamo_Lombardy (CAM) 9.6384 45.869 Whole blood S. Giovenzana
183 ChItCAM25 C. hircus ITALY Valmadrera_Lecco_Lombardy (CAM) 9.3352 45.8287 Whole blood S. Giovenzana
184 ChItCAM26 C. hircus ITALY Valmadrera_Lecco_Lombardy (CAM) 9.3352 45.8287 Whole blood S. Giovenzana
185 ChItCAM27 C. hircus ITALY Valmadrera_Lecco_Lombardy (CAM) 9.3352 45.8287 Whole blood S. Giovenzana
186 ChItCAM28 C. hircus ITALY Malgrate_Lecco_Lombardy (CAM) 9.3563 45.8481 Whole blood S. Giovenzana
187 ChItCAM29 C. hircus ITALY Malgrate_Lecco_Lombardy (CAM) 9.3563 45.8481 Whole blood S. Giovenzana
188 ChItCAM31 C. hircus ITALY Malgrate_Lecco_Lombardy (CAM) 9.3563 45.8481 Whole blood S. Giovenzana
189 ChItCAM32 C. hircus ITALY Vedeseta_Bergamo_Lombardy (CAM) 9.5661 45.899 Whole blood S. Giovenzana
190 ChItCAM33 C. hircus ITALY Vedeseta_Bergamo_Lombardy (CAM) 9.5661 45.899 Whole blood S. Giovenzana
191 ChItVAL02 C. hircus ITALY Avise_Aosta_Valle d’Aosta (VAL) 7.1556 45.7008 Whole blood S. Giovenzana
192 ChItVAL03 C. hircus ITALY Avise_Aosta_Valle d’Aosta (VAL) 7.1556 45.7008 Whole blood S. Giovenzana
193 ChItVAL04 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.0686 45.7643 Whole blood S. Giovenzana
194 ChItVAL05 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.0686 45.7643 Whole blood S. Giovenzana
195 ChItVAL06 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.0686 45.7643 Whole blood S. Giovenzana

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Chapter 4 Goat Domestication

196 ChItVAL07 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.0646 45.7471 Whole blood S. Giovenzana
197 ChItVAL08 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.0646 45.7471 Whole blood S. Giovenzana
198 ChItVAL09 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.0646 45.7471 Whole blood S. Giovenzana
199 ChItVAL10 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.301 45.762 Whole blood S. Giovenzana
200 ChItVAL11 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.301 45.762 Whole blood S. Giovenzana
201 ChItVAL12 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.301 45.762 Whole blood S. Giovenzana
202 ChItVAL13 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.3234 45.7622 Whole blood S. Giovenzana
203 ChItVAL14 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.3234 45.7622 Whole blood S. Giovenzana
204 ChItVAL15 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.3234 45.7622 Whole blood S. Giovenzana
205 ChItVAL16 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.6821 45.6524 Whole blood S. Giovenzana
206 ChItVAL17 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.6821 45.6524 Whole blood S. Giovenzana
207 ChItVAL18 C. hircus ITALY Morgex_Aosta_Valle d’Aosta (VAL) 7.6821 45.6524 Whole blood S. Giovenzana
208 ChItVAL19 C. hircus ITALY Pont st martin_Aosta_Valle d’Aosta (VAL) 7.7817 45.5904 Whole blood S. Giovenzana
209 ChItVAL20 C. hircus ITALY Pont st martin_Aosta_Valle d’Aosta (VAL) 7.7817 45.5904 Whole blood S. Giovenzana
210 ChItVAL21 C. hircus ITALY Pont st martin_Aosta_Valle d’Aosta (VAL) 7.7817 45.5904 Whole blood S. Giovenzana
211 ChItVAL22 C. hircus ITALY Jovencan_Aosta_Valle d’Aosta (VAL) 7.2953 45.7203 Whole blood S. Giovenzana
212 ChItVAL23 C. hircus ITALY Jovencan_Aosta_Valle d’Aosta (VAL) 7.2953 45.7203 Whole blood S. Giovenzana
213 ChItVAL25 C. hircus ITALY Gressan_Aosta_Valle d’Aosta (VAL) 7.3269 45.7193 Whole blood S. Giovenzana
214 ChItVAL26 C. hircus ITALY Gressan_Aosta_Valle d’Aosta (VAL) 7.3269 45.7193 Whole blood S. Giovenzana
215 ChItVAL27 C. hircus ITALY Gressan_Aosta_Valle d’Aosta (VAL) 7.3269 45.7193 Whole blood S. Giovenzana
216 ChItVAL28 C. hircus ITALY Aosta_Aosta_Valle d’Aosta (VAL) 7.3121 45.7845 Whole blood S. Giovenzana
217 ChItVAL29 C. hircus ITALY Aosta_Aosta_Valle d’Aosta (VAL) 7.3121 45.7845 Whole blood S. Giovenzana
218 ChItVAL30 C. hircus ITALY Aosta_Aosta_Valle d’Aosta (VAL) 7.3121 45.7845 Whole blood S. Giovenzana
219 ChItVAL31 C. hircus ITALY Arnad_Aosta_Valle d’Aosta (VAL) 7.6797 45.6577 Whole blood S. Giovenzana
220 ChItVAL32 C. hircus ITALY Arnad_Aosta_Valle d’Aosta (VAL) 7.6797 45.6577 Whole blood S. Giovenzana
221 ChItVAL33 C. hircus ITALY Arnad_Aosta_Valle d’Aosta (VAL) 7.6797 45.6577 Whole blood S. Giovenzana
222 ChItBIO02 C. hircus ITALY Angolo terme_Brescia_Lombardy (BIO) 10.1526 45.8856 Whole blood S. Giovenzana
223 ChItBIO03 C. hircus ITALY Angolo terme_Brescia_Lombardy (BIO) 10.1526 45.8856 Whole blood S. Giovenzana
224 ChItBIO04 C. hircus ITALY Prestine_Brescia_Lombardy (BIO) 10.3211 45.9343 Whole blood S. Giovenzana
225 ChItBIO06 C. hircus ITALY Prestine_Brescia_Lombardy (BIO) 10.3211 45.9343 Whole blood S. Giovenzana
226 ChItBIO08 C. hircus ITALY Ceto_Brescia_Lombardy (BIO) 10.3512 46.0033 Whole blood S. Giovenzana
227 ChItBIO09 C. hircus ITALY Ceto_Brescia_Lombardy (BIO) 10.3512 46.0033 Whole blood S. Giovenzana

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Chapter 4 Goat Domestication

228 ChItBIO10 C. hircus ITALY Ceto_Brescia_Lombardy (BIO) 10.3526 46.005 Whole blood S. Giovenzana
229 ChItBIO12 C. hircus ITALY Ceto_Brescia_Lombardy (BIO) 10.3526 46.005 Whole blood S. Giovenzana
230 ChItBIO13 C. hircus ITALY Ceto_Brescia_Lombardy (BIO) 10.3675 46.0751 Whole blood S. Giovenzana
231 ChItBIO15 C. hircus ITALY Ceto_Brescia_Lombardy (BIO) 10.3675 46.0751 Whole blood S. Giovenzana
232 ChItBIO16 C. hircus ITALY Ceto_Brescia_Lombardy (BIO) 10.3792 46.0792 Whole blood S. Giovenzana
233 ChItBIO17 C. hircus ITALY Ceto_Brescia_Lombardy (BIO) 10.3792 46.0792 Whole blood S. Giovenzana
234 ChItBIO18 C. hircus ITALY Ceto_Brescia_Lombardy (BIO) 10.3792 46.0792 Whole blood S. Giovenzana
235 ChItBIO19 C. hircus ITALY Saviore dell'adamello_Brescia_Lombardy (BIO) 10.4371 46.0702 Whole blood S. Giovenzana
236 ChItBIO20 C. hircus ITALY Saviore dell'adamello_Brescia_Lombardy (BIO) 10.4371 46.0702 Whole blood S. Giovenzana
237 ChItBIO21 C. hircus ITALY Saviore dell'adamello_Brescia_Lombardy (BIO) 10.4371 46.0702 Whole blood S. Giovenzana
238 ChItBIO22 C. hircus ITALY Valle di saviore_Brescia_Lombardy (BIO) 10.4371 46.0702 Whole blood S. Giovenzana
239 ChItBIO23 C. hircus ITALY Valle di saviore_Brescia_Lombardy (BIO) 10.4371 46.0702 Whole blood S. Giovenzana
240 ChItBIO24 C. hircus ITALY Valle di saviore_Brescia_Lombardy (BIO) 10.4371 46.0702 Whole blood S. Giovenzana
241 ChItBIO25 C. hircus ITALY Cevo_Brescia_Lombardy (BIO) 10.4028 46.0721 Whole blood S. Giovenzana
242 ChItBIO27 C. hircus ITALY Cevo_Brescia_Lombardy (BIO) 10.4028 46.0721 Whole blood S. Giovenzana
243 ChItBIO28 C. hircus ITALY Cedegolo_Brescia_Lombardy (BIO) 10.3561 46.0753 Whole blood S. Giovenzana
244 ChItBIO29 C. hircus ITALY Cedegolo_Brescia_Lombardy (BIO) 10.3561 46.0753 Whole blood S. Giovenzana
245 ChItBIO30 C. hircus ITALY Cedegolo_Brescia_Lombardy (BIO) 10.3561 46.0753 Whole blood S. Giovenzana
246 ChItBIO31 C. hircus ITALY Darfo_Brescia_Lombardy (BIO) 10.1945 45.8733 Whole blood S. Giovenzana
247 ChItBIO32 C. hircus ITALY Darfo_Brescia_Lombardy (BIO) 10.1945 45.8733 Whole blood S. Giovenzana

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Chapter 4 Goat Domestication

Supplementary Table 4.3. Additional information about the archeological sites indicated in Fig. 2a.

Origin of early
Site Region Country Culture Date cal. B.P. References
domestic goats
Nevalı Çori Eastern Anatolia Turkey Early PPNB ca. 10,500 local 7
Shillourokambos Cyprus Cyprus Early/Middle PPNB 10,300-10,200 transferred 8,9
Aswad Damascus plain Syria Early/Middle PPNB 10,300-10,000 transferred 10
Çayönü Eastern Anatolia Turkey Middle PPNB ca. 10,000 ? 11
Aşıklı Central Anatolia Turkey Middle PPNB 10,000-9500 ? 12
Nemrik Eastern Anatolia Iraq Middle PPNB 10,000-9500 ? 13
Ganj Dareh Central Zagros Iran Aceramic Neolithic 9900-9700 local 14-16
Halula Euphrates Valley Syria Middle PPNB 9800-9500 transferred 17
Abu Hureyra Euphrates Valley Syria Middle PPNB 9800-9500 transferred 18,19
Tapeh Guran Central Zagros Iran Aceramic Neolithic 9500-9200 ? 14-16
Ali Kosh Zagros lowlands Iran Aceramic Neolithic 9500-9400 transferred 14-16
Tal-i-Mushki Fars Iran Aceramic Neolithic 8000-8500 ? 20
Mehrgahr Indus Valley Pakistan Early Neolithic ?8000-7500 ? 21-23

PPNB: PrePottery Neolithic B

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Chapter 4 Goat Domestication

Supplementary Table 4.4. Partition of the genetic variance among geographic regions and populations by Analysis of molecular
variance for bezoars (Capra aegagrus).

All percentages of variations are significantly different from 0 (*: P< 0.001 ; **: P<0.00001). d.f.: degree of freedom.

Source of variation d.f. Sum of squares Variance components % of variation

Among Regions 7 4079.332 4.89819 9.40**
Among populations
35 8340.091 19.64446 37.70**
within regions
Within populations 444 12240.671 27.56908 52.90*
Total 486 24660.094 52.11173

Supplementary Table 4.5. TMRCA for different mtDNA haplogroups of goats (Capra hircus).

Divergence A versus A haplogroup B haplogroup C haplogroup D haplogroup

C (years) (years) (years) (years) (years)
200,000 55,000 29,000 29,000 36,000
300,000 83,000 44,000 44,000 53,000

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Chapter 4 Goat Domestication

Supplementary Figure 4.1. Number of ancestral haplotypes at the time of

domestication as a function of the size of the sample. The dots correspond to the
bootstrap replicates and the curves have been obtained using a polynomial regression.

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Chapter 4 Goat Domestication

Supplementary Figure 4.2. Pairwise coalescence times of goat (Capra hircus) mtDNA
haplotypes. Genetic distances are computed as the number of differences between pairs of
sequences and are then rescaled in time by using 250,000 years for the divergence time
between A and C haplogroups. The shaded part of the histogram corresponds to the pairs
of sequences that coalesced more recently than the domestication.

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Chapter 4 Goat Domestication

Supplementary Figure 4.3. Probability of observing more than the present number of
individuals from the A haplogroup as a function of the frequency of the individuals
from the A haplogroup at the time of the domestication.

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Chapter 4 Goat Domestication

Supplementary Figure 4.4. Levels of genetic polymorphism of nuclear DNA inferred

from AFLP analysis for the bezoar (Capra aegagrus) and for eight goat (Capra
hircus) breeds, five from Iran, three from Italy.

CAE, C. aegagrus; VAL, Valdostana; BIO, Bionda dell'Adamello; CAM,

Camosclata; RAI, Raini; LOC, Iranian local breeds; KUR, Kurdi; KSH,

Kermanshah; SAN, Sanandaj.

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Chapter 4 Goat Domestication

Supplementary Figure 4.5. Placement of the bezoars of the A haplogroup from the
Lar Mountains (Southeast Iran, locality 33 in Figure 2b) within the phylogeny of the
A haplogroup of goats. The presence of bezoar haplotypes (in green) in many different
clades of the phylogeny indicates a likely introgression from the domestics to the wilds.

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 Chapter 4 Goat Domestication

1. Luikart, G. et al. Multiple maternal origins and weak phylogeographic structure in

domestic goats. Proc. Natl. Acad. Sci. USA 98, 5927-5932 (2001).

2. Fernández, H. et al. Divergent mtDNA lineages of goats in an Early Neolithic site,

far from the initial domestication areas. Proc. Natl. Acad. Sci. USA 103, 15375-
15379 (2006).

3. Tamura, K. & Nei, M. Estimation of the number of nucleotide substitutions in the

control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol.
10, 512-526 (1993).

4. Zeder, M. A., Emshwiller, E., Smith, B. D. & Bradley, D. G. Documenting

domestication: the intersection of genetics and archaeology. Trends Genet. 22, 139-
155 (2006).

5. Xuebin, Q. et al. Genetic diversity and differentiation of Mongolian and Russian yak
populations. J. Anim. Breed. Genet. 122, 117-126 (2005).

6. Jansen, T. et al. Mitochondrial DNA and the origins of the domestic horse. Proc.
Natl. Acad. Sci. USA 99, 10905-10910 (2002).

7. Peters, J., von den Driesch, A. & Helmer, D. in The first steps of animal
domestication. New archaeological approaches (eds Vigne, J.-D., Peters, J. &
Helmer, D.) 96-124 (Oxbow Books, Oxford, UK, 2005).

8. Vigne, J.-D. et al. in Archaeozoology of the Near East IV, Proc. 4th int. Symp.
Archaeozoology of Southwestern Asia and Adjacent Areas (ASWA; Paris, June
1998) (eds Mashkour, M., Choyke, A. M., Buitenhuis, H. & Poplin, F.) 52-75
(Archaeological Research and Consultancy, Groningen, 2000).

9. Vigne, J.-D., Carrère, I. & Guilaine, J. in Le Néolithique de Chypre (eds Guilaine, J.

& Le Brun, A.) 239-251 (Bull. Corr. Hélléniques, Vol. Suppl. 43, 2003).

10. Helmer, D. & Gourichon, L. in Archaeozoology of the Near East VIII, Proc. 4th int.
Symp. Archaeozoology of Southwestern Asia and adjacent areas (eds Vila, E. &
Gourichon, L.) in press (Maison de l’Orient Méditerranéen, Lyon).

11. Hongo, H. & Meadow, R. H. in Archaeozoology of the Near East IV, Proc. 4th int.
Symp. Archaeozoology of Southwestern Asia and adjacent areas (eds Mashkour, M.,
Choyke, A. M., Buitenhuis, H. & Poplin, F.) 121-140 (Archaeological Research and
Consultancy, Groningen, 2000).

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Chapter 4 Goat Domestication

12. Vigne, J.-D. & Buitenhuis, H. Les premiers pas de la domestication animale à
l’Ouest de l’Euphrate : Chypre et l’Anatolie centrale Paléorient 25, 49-62 (1999).

13. Koslowski, S. K. Nemrik 9 - Pre Pottery neolithic site in Iraq, (Inst. Archaeol.,
Warsaw, 1989-99) vol 1-5.

14. Zeder, M. A. & Hesse, B. The initial domestication of goats (Capra hircus) in the
Zagros Mountains 10,000 years ago. Science 287, 2254-2257 (2000).

15. Zeder, M. A. A metrical analysis of a collection of modern goats (Capra hircus

aegagrus and C. h. hircus) from Iran and Iraq: Implications for the study of caprine
domestication. J. Archaeol. Sci. 28, 61-79 (2001).

16. Zeder, M. A. in The First Steps of Animal Domestication. New Archaeological

Approaches (eds Vigne, J.-D., Peters, J. & Helmer, D.) 125-146 (Oxbow Books,
Oxford, UK, 2005).

17. Saña Seguí, M. Arqueología de la domesticaión animal. La gestión de los recursos

animales en Tell Halula (Valle del Éufrates-Siria) del 8.800 al 7.000 BP.
(Universitat Autònoma de Barcelona, Treballs d’Arqueologia del Pròxim Orient 1.
Barcelona, 1999) pp. 241.

18. Legge, A. J. in The origins and spread of agriculture and pastoralism in Eurasia (ed
Harris, D. R.) 238-262(Smithsonian Institution Press, Washington D.C., 1996).

19. Moore, A. M. T., Legge, A. J. & Hillman, G. C. Village on the Euphrates (Oxford
University Press, Oxford USA, 2000).

20. Mashkour, M. in The Origins of State Organizations in Prehistoric Highland Fars,

Excavations atT all-e Bakun (ed Alizadeh, A.) 101-105 (Oriental Institut
Publications 128, Chicago. Illinois, 2006).

21. Meadow, R. H. in South Asian Archaeology 1979 (ed Härtel, H.) 143-179 (Dietrich
Reimer Verlag, Berlin, 1981).

22. Meadow, R. H. in South Asian Archaeology 1981 (ed Allchin, B.) 34-40 (Cambridge
University press, Cambridge, 1984).

23. Meadow, R. H. in The origins and spread of agriculture and pastoralism in Eurasia
(ed Harris, D. R.) 390-412 (Smithsonian Institution Press, Washington D.C., 1996).

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 Chapter 4 Goat Domestication

Supplementary Figure 4.6. The habitat of Capra aegagrus in Dahaj protected area in
Iran (Photo by Saeid Naderi).

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Chapter 5. Are cattle, sheep, and
goats endangered species?
Chapter 5 Are cattle, sheep, and goats endangered species?

Chapter 5. Are cattle, sheep, and goats endangered species?

P. Taberlet1, A. Valentini2, H. R. Rezaei1,3, S. Naderi1,4, F. Pompanon1, R. Negrini5, P.

Ajmone-Marsan5,6

Molecular Ecology: (2008) 17, 275–284

1
Laboratoire d'Ecologie Alpine, CNRS-UMR 5553, Université Joseph Fourier, BP 53,
38041 Grenoble Cedex 09, France.
2
Dipartimento di Produzioni Animali, Università della Tuscia, via de Lellis, 01100
Viterbo, Italy.
3
Environmental Sciences Department, Gorgan University of Agriculture and Natural
Resources, P.O. Box 386, Gorgan, Iran.
4
Natural Resources Faculty of Guilan University, Guilan, Iran.
5
Istituto di Zootecnica, Università Cattolica del S. Cuore, via E. Parmense, 84, 29100
Piacenza, Italy.
6
and the Econogene Consortium ([Link])

Keywords: breeds, conservation genetics, genetic diversity, livestock

Corresponding author: P. Taberlet, Laboratoire d'Ecologie Alpine, CNRS-UMR 5553,

Université Joseph Fourier, BP 53, 38041 Grenoble Cedex 09, France; Tel: +33(0)4 76 51
45 24; Fax: +33(0)4 76 51 42 79; E-mail: [Link]@[Link]

Running title: Are cattle, sheep, and goats endangered species?

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Chapter 5 Are cattle, sheep, and goats endangered species?

Abstract

For about 10000 years, farmers have been managing cattle, sheep, and goats in a
sustainable way, leading to animals that are well adapted to the local conditions. About
two hundreds years ago, the situation started to change dramatically, with the rise of the
concept of breed. All animals from the same breed began to be selected for the same
phenotypic characteristics, and reproduction among breeds was seriously reduced. This
corresponded to a strong fragmentation of the initial populations. A few decades ago, the
selection pressures were increased again in order to further improve productivity, without
enough emphasis on the preservation of the overall genetic diversity. The efficiency of
modern selection methods successfully increased the production, but with a dramatic loss
of genetic variability. Many industrial breeds now suffer from inbreeding, with effective
population sizes falling below 50. With the development of these industrial breeds came
economic pressure on farmers to abandon their traditional breeds, and many of these have
recently become extinct as a result. This means that genetic resources in cattle, sheep, and
goats are highly endangered, particularly in developed countries. It is therefore important
to take measures that promote a sustainable management of these genetic resources, first
by in situ preservation of endangered breeds, second by using selection programs to
restore the genetic diversity of industrial breeds, and finally by protecting the wild
relatives that might provide useful genetic resources.

Introduction

According to the Food and Agriculture Organization of the United Nations (FAO),
the population sizes of domestic cows, sheep, and goats, are about 1,400, 1,100, and 700
million, respectively (Scherf 2000; Table 5.1). Over the past 15 years, about 300 of 6000
breeds of farm animals identified by the FAO have become extinct. Furthermore, 1350
breeds of domestic animals currently face extinction in the near future (Scherf 2000). This
trend of loss of cattle, sheep, and goat breeds appears particularly strong in Europe (Table
5.1), possibly because it remains poorly documented in developing countries. At the
worldwide level, 17% of cattle and 14% of sheep breeds have already been lost (Scherf
2000).

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Chapter 5 Are cattle, sheep, and goats endangered species?

Table 5.1. Population sizes, current number of breeds, number of extinct breeds for cattle,
sheep, and goats in different regions (source: FAOSTAT from Scherf (2000); statistics
concerning 170 countries).

Cattle Sheep Goat

Africa Population size ('000) 174 556 127 440 137 104
Current number of breeds 251 147 89
Number of extinct breeds 23 8 0
Asia and Pacific Population size ('000) 461 197 408 098 390 433
Current number of breeds 236 233 146
Number of extinct breeds 19 7 1
Europe Population size ('000) 162 119 185 035 26 092
Current number of breeds 482 629 187
Number of extinct breeds 171 142 14
Latin America Population size ('000) 356 069 89 372 40 752
and Caribbean
Current number of breeds 107 42 34
Number of extinct breeds 24 0 0
Near East Population size ('000) 71 913 242 770 114 572
Current number of breeds 86 201 94
Number of extinct breeds 12 11 1
North America Population size ('000) 141 481 7 891 1 428
Current number of breeds 62 61 20
Number of extinct breeds 5 13 1
Total population size ('000) 1 367 335 1 060 606 710 381

The International Union for the Conservation of Nature and Natural Resources
(IUCN) regards a species as critically endangered, endangered, or vulnerable when its
effective population size falls below 50, 250, or 1000, respectively (IUCN 2000). The
rule-of-thumb in conservation biology considers that the effective population size should
not be lower than 50 to avoid extinction in the short-term, and not lower than 500 to avoid
extinction in the long term (Franklin 1980).
Thus, it seems irrelevant to consider these three domestic species as endangered,
considering their numbers that in the case of random mating result in effective population
sizes way above the critical thresholds. However, such conclusions based purely on the

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Chapter 5 Are cattle, sheep, and goats endangered species?

number of individuals are often overly simplistic. After a brief presentation of the
domestication history of these three species, we will separately consider the cases of
highly productive breeds and of local breeds with low population sizes. We will examine
the potential threats that cattle, sheep, and goats might suffer from, with emphasis on the
current management, particularly in developed countries. These three domestic species are
divided into many breeds (Table 5.1), and each breed can be considered as an independent
genetic unit, as crosses are not usually employed for reproduction in developed countries.
Is the current management of breeds of high commercial value sustainable? What is the
impact of managing these breeds separately, of the extensive use of artificial insemination,
and of increasing the selection pressure for higher production? What are the optimal
management guidelines for a sustainable use of genetic resources in cattle, sheep, and
goats?
From a conservation biology point of view, our goal is also to show the possible
parallel between domestic and wild species. Do domestic and wild species suffer from the
same threats? Should the same concepts be used for managing wild and domestic animals?

Wild ancestors and the domestication process

Beside the wild ancestor when it still exists, the breeds to be used as genetic
resources (i.e. the breeds with the highest genetic diversity) are expected to be found close
to the domestication centres. As a consequence, precise knowledge of wild ancestors, of
domestication centres, and of colonization routes is of prime importance for tracking
genetic resources.
Information about cattle, sheep, and goat domestication comes from archaeological
evidence, mostly from osteometry and morphometry, but also from genetic data (Vigne et
al. 2005). Up to now, genetic studies on domestication mainly concerned the analysis of
mitochondrial DNA (mtDNA) polymorphisms, either in the domestic species itself, or by
comparing the domestic species with its wild ancestor.

Cattle

It is now widely recognized that the wild ancestor of all domesticated cattle was the
auroch (Bos primigenius) (Zeuner 1963). The aurochs are now extinct. For domestic cattle,
the common usage accepts two taxa (Bos taurus and B. indicus) that fully interbreed. B.

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Chapter 5 Are cattle, sheep, and goats endangered species?

indicus differs from B. taurus by the presence of a prominent hump. The mtDNA
polymorphism reflects this dichotomy (Fig. 5.1), but the reality is much more complex due
to extensive hybridization among these two cattle haplogroups in Africa (Bradley et al.
1996).
The presence of two mtDNA haplogroups is interpreted as an indication of two main
domestication events, one in the Fertile Crescent leading to B. taurus, and one in the
Indian sub-continent leading to B. indicus (Loftus et al. 1994; Bradley et al. 1996; Bradley
& Magee 2006). Eighty four percent of the mitochondrial variation is partitioned among
Europe, Asia, and Africa (Bradley et al. 1996). The earliest archaeological evidence of
cattle domestication dates from 8800 to 8300 BC (calibrated) in the Fertile Crescent
(Helmer et al. 2005).

Sheep

Archaeological evidence indicates that domestic sheep, Ovis aries, were also
domesticated in the Fertile Crescent, circa 8500 BC (calibrated) (Peters et al. 2005).
However, their wild ancestors have not yet been identified with certainty, as no extensive
genetic studies have been carried out on the putative ancestors. The wild candidates are
Ovis gmelini (the Asiatic mouflon), O. vignei (the urial), and O. ammon (the argali), with a
preference for O. gmelini, which shows the same chromosomal numbers as the domestic
species (Bruford & Townsend 2006).
To date, four main mitochondrial DNA haplogroups have been found in domestic
sheep, indicating multiple maternal origins (Fig. 5.1), and 35% of the mtDNA variation is
partitioned among continents (Townsend 2000, cited by Bruford et al. 2003).

Goats

Goat domestication is very well documented. The first archaeological evidence traces
back as far as 8500-7900 BC (calibrated) in the Zagros mountains (Fertile Crescent)
(Zeder 2005), and the wild ancestor is the bezoar, Capra aegagrus (Fernández et al. 2005;
Luikart et al. 2006).
The main characteristic of goat mtDNA polymorphism is its large haplotypic
variation and its weak intercontinental phylogeographic structure, with only 10%
partitioned among continents, suggesting high historical gene flow among continents

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Chapter 5 Are cattle, sheep, and goats endangered species?

(Luikart et al. 2001). A recent ancient DNA study suggested that high gene flow already
occurred during the Neolithic expansion into Europe (Fernández et al. 2006). Up to now,
five different mtDNA haplogroups have been found (Fig. 5.1), indicating multiple
maternal origins, as in sheep and cattle.

Dispersal from the domestication centres

During the 3000-4000 years following the initial domestication events in the Fertile
Crescent, agriculture spread over Europe, Africa, and Asia. Archaeological evidence
showed that two main colonization routes took place in Europe (Fig. 5.2): the
Mediterranean route and the Danubian route. A decrease of genetic diversity likely
occurred during this colonization process in Europe. This has been demonstrated for cattle
mtDNA, for which populations in Western Europe exhibit lower polymorphism than those
in the Near East (Troy et al. 2001; Bradley & Magee 2006). A number of secondary
livestock migrations accompanied human migrations in more recent historical times and
contributed to the shaping of local gene pools. For instance an introgression of the African
gene pool is observed in Iberian cattle breeds (Cymbron et al. 1999; Miretti et al. 2004;
Anderung et al. 2005; Beja-Pereira et al. 2006), possibly linked to the Moorish occupation
or to even earlier events. Also, a surprisingly high level of mtDNA variation and close
genetic relationship was discovered between Tuscan cattle breeds and Near Eastern
breeds. This pattern might be linked either to the sailing and docking in Tuscany of
Middle Eastern people in the late Bronze Age and to the onset of the Etruscan civilization
in Central Italy (Pellecchia et al. 2007), or to an introgression from local aurochs (Beja-
Pereira et al. 2006).
Overall, the level of mtDNA polymorphism in cattle, sheep, and goats (Fig. 5.1) is
high, and contains evidence of multiple maternal origins. Such multiple origins correspond
either to several domestication events in different locations and/or at different periods, or
to the capture of several mtDNA haplotypes during a single domestication event.
Furthermore, nuclear DNA polymorphism seems high (see e.g. Maudet et al. 2002),
comparable to what is found in wild species. During crop domestication, many species
went through a strong bottleneck (see references in Zeder 2006), but this is clearly not the
case for livestock. All the current evidence suggests that cattle, sheep, and goats have very
large gene pools on which human induced-selection was acting to produce the very large
diversity of breeds we observe today.

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Chapter 5 Are cattle, sheep, and goats endangered species?

Figure 5.1. Unrooted neighbor-joining trees showing the mtDNA polymorphism of cattle,
sheep, and goats. The phylogenetic analyses were conducted using MEGA version 3.1,
Kumar et al. 2004, with control region sequences. A total of 744 sequences from Loftus et
al. 1994, Bradley et al.1996, and Troy et al. 2001 were used for cattle. A total of 640
sequences from Wood & Phua 1996, Hiendleder et al. 1998, Guo et al. 2005, Pedrosa et
al. 2005, Meadows et al. 2006, and Tapio et al. 2006 were used for sheep. A total of 1813
sequences from Luikart et al. 2001, Sultana et al. 2003, Joshi et al. 2004, Azor et al. 2005,
Chen et al. 2005, Odahara et al. 2005, Pereira et al. 2005, Li et al. 2006, Sardina et al.
2006, and Liu et al. 2007 were used for goats. The letters A, B, C, etc. in the trees for
sheep and goats represent the different mtDNA haplogroups described in the literature.

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Chapter 5 Are cattle, sheep, and goats endangered species?

Figure 5.2. The two main initial advancements of the Neolithic culture into Europe (from
Fernàndez et al. 2006). The dates on the map are calibrated radiocarbon date-derived BP,
and correspond to the arrival of agriculture in the corresponding region.

The threats on highly productive breeds

Fragmentation into discrete breeds

About 10000 years ago, farmers started controlling the reproduction of their animals,
by favouring the reproduction of animals with preferred phenotypes, and using males
either from their own farm, or from another farm located in the same area. As a
consequence, farm animals slowly became locally adapted. About two hundred years ago,
the situation started to dramatically change. Stronger selection pressures were applied to
local populations followed by standardization of the desired conformation and
performance. The first cattle herd book was published in Britain in 1822 (Epstein &
Mason 1984). This led to the concept of breed. All animals from the same breed began to
exhibit the same phenotypic characteristics, and reproduction among different phenotypes
(i.e. among different breeds) was seriously reduced. A few decades ago, selection
pressures were increased again in order to further improve productivity. To summarize,
farm animals underwent relatively low selection pressures during about 98% of their

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Chapter 5 Are cattle, sheep, and goats endangered species?

common history with humans, and later their populations were suddenly fragmented into
many well-defined breeds, with high selection constraints.

Effects of artificial insemination and other reproductive technologies

Artificial insemination offers the possibility of easily obtaining thousands of progeny

from a single sire, permitting the dissemination of valuable genes (Vishwanath 2003). It is
widely used in cattle, particularly in dairy farms, and is the main method of reproduction
in many breeds in the developed world, while in sheep and goats it is limited to a few
highly productive breeds. This has greatly sped up the rate of genetic change of livestock
populations by increasing the selection pressure and the reliability of sire breeding values,
estimated from the performance of a large number of relatives. "Improved" germplasm has
flooded almost every market, displacing locally adapted populations and inducing the loss
of many genetic variants.
The effect of artificial insemination on effective population size is sometimes striking
(Table 5.2). For example, Ne is as low as 46 in French Holstein, a breed that counts 2.5
million animals across France (Boichard et al. 1996). An even more extreme result was
found in Japan, where the Japanese Black cattle had a Ne of 17.2 in between 1993 and
1997, despite a census size of 0.53 million reproductive cows (Nomura et al. 2001). A
reduction in effective population size has also been documented in sheep (Maiwashe &
Blackburn 2004; Tapio et al. 2005), and is probably occurring in goat breeds where
artificial insemination has been implemented. Surprisingly, rather high levels of genetic
diversity at the nuclear DNA level still appear to exist in the Holstein cattle population,
with observed heterozygosity above 0.6 (0.67 in Maudet et al. 2002; 0.61 in Vallejo et al.
2003). Such a level of heterozygosity is probably highly overestimated due to an
ascertainment bias produced by non-random sampling of the genetic markers used (Rogers
& Jorde 1996). The microsatellites used were selected among a large set of potential
markers, with the goal of maximizing the level of polymorphism and/or heterozygosity.
They are probably mainly located in chromosomal regions that have not been under
selection. The markers that are either monomorphic or have a low level of polymorphism
are simply ignored and are usually not reported in the literature.

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Chapter 5 Are cattle, sheep, and goats endangered species?

Table 5.2. Examples of effective population sizes in some cattle breeds.

Census Effective
Cattle breed Country Period population population Reference
sizea size (Ne)
Sørensen et al.
Holstein Denmark 1983-1992 - 68
2005
Koenig &
Holstein Germany 1999 ≈ 2,200,000 52
Simianer 2006
Sørensen et al.
Holstein Denmark 1993-2003 ≈ 3,700,000 49
2005
Boichard et al.
Holstein France 1988-1991 (?) ≈ 2,500,000 46
1996
Holstein USA 1999 ≈ 8,500,000 39 Weigel 2001
Sørensen et al.
Jersey Denmark 1977-1991 - 87
2005
Sørensen et al.
Jersey Denmark 1993-2003 ≈ 640,000 53
2005
Jersey USA 1999 ≈ 550,000 30 Weigel 2001
Sørensen et al.
Danish red Denmark 1977-1998 - 157
2005
Sørensen et al.
Danish red Denmark 2001-2003 ≈ 560,000 47
2005
Japanese Nomura et al.
Japan 1986-1990 - 30
black 2001
Japanese Nomura et al.
Japan 1993-1997 ≈ 530,000 17
black 2001
Boichard et al.
Montbéliarde France 1988-1991 (?) ≈ 700,000 125
1996
Boichard et al.
Abondance France 1988-1991 (?) ≈ 65,000 106
1996
Boichard et al.
Normande France 1988-1991 (?) ≈ 800,000 47
1996
Boichard et al.
Tarentaise France 1988-1991 (?) ≈ 14,000 27
1996
a
The census population sizes were obtained either from the cited references, or from other
sources such as breeder associations.

Another problem could be the oversimplification of the models for estimating genetic
values, only involving simple linear models that do not consider interactions between
factors. As a consequence, they do not take into account dominance and epistasis effects,
thus overestimating the genetic value of heterozygotes which are consequently more likely
to be selected for reproduction (Cappuccio et al. 2003). Nevertheless, attention needs to be
paid to the maintenance of sufficient within breed genetic diversity, to preserve

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populations from falling into the extinction vortex (Soulé & Mills 1998) and guarantee the
long-term sustainable exploitation of livestock.
Inbreeding has always been avoided by breeders. Traditional practices included the
exchange of parents among herds, culling of parents when daughters became sexually
mature or confinement in breeding groups with mating with alternate males. Artificial
insemination made these practices unfeasible. Most semen doses in the market arise from
related bulls and this information is not easily available to single breeders, so unwanted
inbreeding is likely to occur; semen doses are available for a long time after a bull is dead,
making an insemination with its descendants more likely; most pedigrees do not go back
more than three generations and therefore grouping females according to the common
recent ancestry will not prevent mating with a relative male.
Artificial selection always reduces the number of genetic variants passed on to the
following generation and with time it leads to the fixation of the desired alleles. The high
level of linkage disequilibrium observed in livestock species (Farnir et al. 2000; Khatkar
et al. 2006) may favour additional fixation of rather large chromosome regions flanking
genes under intense selection, by the hitch-hiking process (Maynard Smith & Haigh
1974). Also, random sampling of a few parents as with artificial insemination may lead to
fixation of genes unlinked to the gene under selection by chance. The selection schemes
currently employed in cattle may make the fixation process particularly rapid. In practice,
young bulls enter the progeny test scheme on a pedigree index computed by the BLUP-
Animal Model (Henderson et al. 1959). The index is built by using the genetic value of
relatives weighted by their relatedness with the candidate bull. Therefore, young bulls
belonging to a family with good records are more likely to be included in the progeny test
program. In this way the genetic pool of the group of parents of the next generation is
dramatically reduced, even before genetic evaluation. After the progeny test, genetic
indexes are computed with the same statistical procedure. Although the contribution of
relatives has less weight here since records of the candidate (or that of its daughters) are
considered as well, bulls in a "good" family still tend to have better indexes.
Consequently, allelic variants are lost in an exponential way by the combination of
selection and of preferential choice across families.
Increasing the selection pressure by the use of a lower number of sires per generation
results in the reduction of the effective population size (Ne, see above) and the increase of
inbreeding, which has short-term negative effects on productivity, particularly on
reproductive traits. Hence it is not surprising that in highly selected dairy cattle breeds, a

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Chapter 5 Are cattle, sheep, and goats endangered species?

continuous and alarming decrease in fertility has been observed in the last 10 to 20 years
in countries in which fertility traits are not sufficiently taken into consideration in the
selection objectives (e.g. Lucy 2001). In addition, inbreeding can promote the emergence
of new hereditary diseases, such as the "complex vertebral malformation" (Mahler et al.
2006), which have strong detrimental economic effects on farms.
Artificial insemination has also dramatically changed the sex ratio, particularly in
dairy cattle breeding, since its introduction into current practice in the past century. The
ratio has declined from 1 to 10-30 males/females to 1 to several hundred (Rabasa 1950). A
very low sex ratio leads to a strong reduction of the effective population size, and thus to
inbreeding.

The threats on local breeds with low population sizes

Socio-economic context

The major threats to livestock genetic diversity result from systemic, regional and
global economic forces and changing agricultural practices. Intensification of production
systems, including the wider availability of vaccines and therapeutics against endemic
diseases, promotes the use of higher-production, less well-adapted genotypes. These facts,
combined with the progressive abandonment of agriculture in marginal areas and the
success of industrial breeding, have led farmers to partially or completely abandon a
number of autochthonous breeds. The lack of application of methods for estimating the
real economic value of these breeds, beside the value of meat, milk, and wool production,
is also partially responsible for this trend (Roosen et al. 2005). As a consequence, many
locally adapted populations have been greatly reduced, posing the new problems of
genetic drift and inbreeding to their ranchers.

Management of small size populations

Data collected within the Econogene EU project on sheep and goat diversity in
marginal areas indicates the presence of significant inbreeding in most of the breeds
investigated despite the scarce use of reproductive technologies (Cañon et al. 2006; Peter
et al. 2007). This is likely due to poor breeding management of frequently small herds. An
insufficient rotation of bucks/rams across farms leads to partial isolation and
fragmentation at the farm, and additionally, the breed level. Hence, in addition to

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Chapter 5 Are cattle, sheep, and goats endangered species?

economic issues, and the disinterest of modern youth in agricultural careers, cultural
barriers further increase the risk of loss of diversity in livestock species.
Populations with a limited number of individuals are particularly difficult to manage
with the aim of maintaining an acceptable level of inbreeding. A strong social/economic
network in the past allowed the exchange of parents as a source of “new blood” for
restoring diversity within herds. Even during Roman times parents were actively traded
and “foreign” parents were highly appreciated (Columella circa 60). Currently, several
barriers to live animal trade are imposed to avoid the spread of highly infectious diseases
(blue tongue, swine fever, etc.). Breeders therefore orientate their choice towards artificial
insemination or parents from a few certified sources, increasing the likelihood of
inbreeding. Breeders Associations could provide technical assistance to these breeders, but
it is understandable that they pay more attention to high value breeds and large farms than
to small size populations. The situation across Europe is however varied, with some non-
profit organisations very active in sustaining small populations, such as the Rare Breeds
Survival Trust in UK. The Italian Breeders Associations (a quasi non-profit organization)
host herd books for smaller populations (e.g. Grigia, Burlina) and provide mating plans
that avoid inbreeding. However, even such well-intentioned efforts cannot guarantee the
long-term survival of all endangered breeds.

Threats to adaptation

Adaptive traits may be rapidly lost by poorly designed crossbreeding leading to

dilution of local genetics by exotic germplasm. Crossbreeding to a more productive breed
from elsewhere, most often a high production breed, is widespread and can destroy the
specific features of an indigenous breed within a few generations. The case of
tripanotolerant livestock breeds in West Africa represents a good example of local
adaptation that might be disrupted by crossbreeding (Agyemang 2005). Recovery from
such loss of distinctiveness can be extremely difficult, requiring many generations of
backcrossing to purebred indigenous animals. In some cases recovery is impossible
because no purebred animals remain to allow a backcrossing recovery program (for
instance, there are so few pure breed Maremmana cattle remaining today in Central Italy,
that even crosses are granted the label of certification of origin). A number of examples
exist, particularly in developing countries, where indiscriminate repeated cross-breeding

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Chapter 5 Are cattle, sheep, and goats endangered species?

quickly disrupted generations of natural and anthropic selection for adaptation to harsh
environments.
Traits such as resistance to local infectious and parasitic diseases, adaptation to poor
forage, homing and gregarious behaviour, which represent key traits for the survival and
management of herds in extensive farming, can be rapidly lost and difficult to rescue. An
example of this effect can be found in Corsica, where local goats, when crossed to Alpine
or Saanen breeds loose their gregarious and homing behaviour and get lost in the
mountains where they are raised in free range. Another example is the Red Maasai sheep
in Kenya, renowned for its hardiness and disease resistance, especially its resistance to
gastrointestinal parasites (Baker et al. 1998). In the mid 1970’s a subsidised dissemination
program for Dorper rams was established in Kenya. Widespread indiscriminate
crossbreeding followed. No instructions were supplied to farmers about how to maintain a
continuous crossbreeding program and many farmers continued crossing their flocks to
Dorpers, which subsequently proved unsuitable in many production areas (Consultative
Group on International Agricultural Research Science Council 2005).

Geographic confinement

When the traditional rearing area is geographically limited, an additional risk is

represented by highly contagious infectious diseases that may wipe out an entire
population if back-ups do not exist elsewhere. This was the case of the Herdwick sheep
breed in UK, almost exterminated recently by the foot and mouth disease epidemics in
2001 (Alderson 2001).
Several methods are proposed for conservation of farm animal genetic resources.
They may be in vitro, through the cryo-preservation of animal gametes, embryos and
tissues or in vivo, by conserving animal flocks ex-situ, that is outside their place of origin,
for example in experimental farms, or in situ, that is within their natural environmental
and socio-economic context. When the conservation of adaptive traits in a changing
environment is the actual aim, in situ conservation is the best option.

Conclusion

Domestic animals are currently losing genetic diversity through many mechanisms.
First, the highly productive breeds have recently been intensively selected for production

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Chapter 5 Are cattle, sheep, and goats endangered species?

traits, without enough emphasis on the preservation of the overall genetic diversity. Many
breeds in developed countries suffer from a very low effective population size despite their
total number of individuals. The strong decrease in fertility of the Holstein cattle, as well
as the recent emergence of new hereditary diseases, is a sign that inbreeding is becoming a
serious threat in the short term. Second, autochthonous breeds in marginal areas are also
seriously endangered. Farmers are often obliged to abandon their traditional breeds and to
raise more competitive industrial breeds. As a consequence, many locally adapted breeds
have already disappeared (Table 5.1). Furthermore, even in less developed countries, the
introgression of genes from industrial breeds seriously compromises the long-term
persistence of genetic resources in locally well-adapted breeds.
Many parallels can be found in issues related to threats and conservation of domestic
and wild animal species. One of the most problematic threats to wild populations is the
fragmentation due to human activity (Frankham et al. 2002). Habitat fragmentation
induces the risk of excessive genetic drift and inbreeding in isolated populations. In
domestic species, fragmentation is mainly due to human intervention that blocks gene flow
across populations by keeping breeds as separate breeding units. In non-industrial breeds
the diffused cultural inability to properly manage small size populations may lead to
fragmentation and isolation even at the farm level.
In conservation biology, it is well known that the long-term viability of populations
is directly linked to its effective population size. A reduction of the effective population
size to below 50 seriously compromises the short-term survival of a wild population. This
problem is exacerbated in industrial domestic breeds.
The real value of biodiversity is difficult to assess. This is true for wild species (e.g.
Myers 1996), but also for domestic animals. Most of the difficulties in preserving the
diversity of domestic animals are due to a short-term evaluation of the economic value that
promotes the exclusive use of industrial breeds. Furthermore, preservation of genetic
resources in domestic animals does not have the same image for the public as preserving
the giant panda or whales. Domestic animals have been selected and modified by humans.
They do not bear the same "natural" perception that wild species have for the public,
despite being our food. This is a paradox, because our future will undoubtedly be linked to
our ability to produce food from domestic animals. The fact that domestic animals are
numerous, and that we have full control on their reproduction make it difficult to explain
that some breeds are endangered and that we are losing valuable genetic resources.

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Chapter 5 Are cattle, sheep, and goats endangered species?

In light of the current loss of genetic diversity in farm animals, it is extremely

important to take measures that promote a sustainable management of these genetic
resources. These measures must prioritize the in situ preservation of endangered breeds,
and selection programs that will restore the genetic diversity in industrial breeds. Ex situ
conservation is not suitable, as it relaxes the traditional selection pressures and would not
allow the preservation of the genetic resources of interest. In the same way, cryo-
conservation should only represent a very short-term strategy in case of emergency. The
situation is exacerbated by the fact that we do not know which feature will be useful to
exploit in the future, and which breed carries this feature today.
Beside the sustainable management of domestic species themselves, it is also
extremely important to take care of the wild relatives and of the wild ancestors when they
still exist. The wild ancestor of cattle is already extinct, and the closest wild relatives are
vulnerable (Bos frontalis), endangered (B. javanicus), or critically endangered (B. sauveli);
the putative wild ancestors of sheep and goats are all vulnerable or endangered (according
to IUCN classification).
Concerning less productive breeds, the price of their products should take into
account their value as storage of unique genetic diversity. The public should be made
aware of this before any strategies for the sustainable management of livestock genetic
resources are implemented. Therefore, in opposition to the rules of the global market,
subsidies should be given to help farmers who contribute to the preservation of genetic
resources in marginal or rare breeds. The Doha agreement (World Trade Organisation
2001) took this issue partially into consideration in permitting state subsidies for typical
agricultural products. However this decision was only taken because of the marginal
volume of this niche in comparison to the overall market.
Although cattle, sheep, and goats cannot be considered as endangered species
according to the number of individuals, it is clear that many breeds are highly endangered,
and that we are losing genetic resources. In a few decades, we might lose most of the
highly valuable genetic resources that humanity has gradually selected over the past
10,000 years. Despite many conservation programs implemented by the FAO, the
conservation of many locally adapted breeds opposes the short-term economic profit.
Sadly, the erosion of livestock genetic resources is still continuing, and the same
observation has also been made for crops (Esquinas-Alcazar 2005).

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Chapter 5 Are cattle, sheep, and goats endangered species?

References

Agyemang K (2005) Trypanotolerant livestock in the context of trypanosomiasis

intervention strategies. PAAT Technical and Scientific Series n°7, Food and
Agriculture Organization of the United Nations, Rome.
Alderson L (2001) Foot-and-mouth disease in the United Kingdom 2001; its cause, course,
control and consequences. RBI/EAAP/FAO meeting, Budapest, 23 August 2001.
Anderung C, Bouwman A, Persson P, et al. (2005) Prehistoric contacts over the Straits of
Gibraltar indicated by genetic analysis of Iberian Bronze Age cattle. Proceedings
of the National Academy of Sciences of the United States of America, 102, 8431-
8435.
Azor PJ, Monteagudo LV, Luque M, et al. (2005) Phylogenetic relationships among
Spanish goats breeds. Animal Genetics, 36, 423-425.
Baker RL, Mwamachi DM, Audho JO, Aduda EO, Thorpe W (1998) Resistance of Galla
and Small East African goats in the sub-humid tropics to gastrointestinal nematode
infections and the peri-parturient rise in faecal egg counts. Veterinary
Parasitology, 79, 53-64.
Beja-Pereira A, Caramelli D, Lalueza-Fox C, et al. (2006) The origin of European cattle:
evidence from modern and ancient DNA. Proceedings of the National Academy of
Sciences of the United States of America, 103, 8113-8118.
Boichard D, Maignel L, Verrier E (1996) Analyse généalogique des races bovines laitières
françaises. INRA Productions Animales, 9, 323-335.
Bradley DG, MacHugh DE, Cunningham P, Loftus R (1996) Mitochondrial diversity and
the origins of African and European cattle. Proceedings of the National Academy
of Sciences of the United States of America, 93, 5131-5135.
Bradley DG, Magee DA (2006) Genetics and origins of domestic cattle. In: Documenting
domestication. New genetics and archaeological paradigms (eds. Zeder MA,
Bradley DG, Emshwiller E, Smith BD), pp. 317-328. University of California
Press, Ltd, Berkeley, CA.
Bruford M, Bradley D, Luikart G (2003) DNA markers reveal the complexity of livestock
domestication. Nature Reviews Genetics, 3, 900-910.
Bruford MW, Townsend SJ (2006) Mitochondrial DNA diversity in modern sheep:
implications for domestication. In: Documenting domestication. New genetics and

- 167 -
Chapter 5 Are cattle, sheep, and goats endangered species?

archaeological paradigms (eds. Zeder MA, Bradley DG, Emshwiller E, Smith

BD), pp. 306-316. University of California Press, Ltd, Berkeley, CA.
Cañon J, Garcia D, Garcia-Atance MA, et al. (2006) Geographical partitioning of goat
diversity in Europe and the Middle East. Animal Genetics, 37, 327-334.
Cappuccio I, Pariset L, Valentini A (2003) Is artificial selection in Italian Holstein Friesian
cattle favouring heterozygotes? Italian Journal of Animal Science, 2, 115-117.
Chen SY, Su YH, Wu SF, Sha T, Zhang YP (2005) Mitochondrial diversity and
phylogeographic structure of Chinese domestic goats. Molecular Phylogenetics
and Evolution, 37, 804-814.
Columella LIM (circa 60) De re rustica, liber VII II. De ovibus emendis tuendisque
[Link]
Consultative Group on International Agricultural Research Science Council (2005)
Conservation of Livestock and Fish Genetic Resources, Joint report of two studies
commissioned by the CGIAR Science Council.
Cymbron T, Loftus RT, Malheiro MI, Bradley DG (1999) Mitochondrial sequence
variation suggests an African influence in Portuguese cattle. Proceedings of the
Royal Society of London Series B-Biological Sciences, 266, 597-603.
Epstein H, Mason IL (1984) Cattle. In: Evolution of domesticated animals (ed. Mason IL),
pp. 6-27. Longman Inc., New York.
Esquinas-Alcazar J (2005) Protecting crop genetic diversity for food security: political,
ethical and technical challenges. Nature Reviews Genetics, 6, 946-953.
Farnir F, Coppieters W, Arranz JJ, et al. (2000) Extensive genome-wide linkage
disequilibrium in cattle. Genome Research, 10, 220-227.
Fernández H, Hugues S, Vigne JD, et al. (2006) Divergent mtDNA lineages of goats in an
Early Neolithic site, far from the initial domestication areas. Proceedings of the
National Academy of Sciences of the United States of America, 103, 15375-15379.
Fernández H, Taberlet P, Mashkour M, Vigne JD, Luikart G (2005) Assessing the origin
and diffusion of domestic goats using ancient DNA. In: The first steps of animal
domestication. New archaeological approaches (eds. Vigne JD, Peters J, Helmer
D), pp. 50-54. Oxbow Books, Oxford, UK.
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics
Cambridge University Press, Cambridge, UK.
Franklin IR (1980) Evolutionary changes in small populations. In: Conservation biology:
an evolutionary-ecological perspective (eds. Soulé ME, Wilcox BA), pp. 135-149.

- 168 -
Chapter 5 Are cattle, sheep, and goats endangered species?

Sinauer, Sunderland, MA.

Guo J, Du LX, Ma YH, et al. (2005) A novel maternal lineage revealed in sheep (Ovis
aries). Animal Genetics, 36, 331-336.
Helmer D, Gourichon L, Monchot H, Peters J, Segui MS (2005) Identifying early
domestic cattle from pre-pottery Neolithic sites on teh Middle Eurphrates using
sexual dimorphism. In: The first steps of animal domestication. New
archaeological approaches (eds. Vigne JD, Peters J, Helmer D), pp. 86-95. Oxbow
Books, Oxford, UK.
Henderson CR, Kempthorne O, Searle SR, Von Krosigk CN (1959) Estimation of
environmental and genetic trends from records subject to culling. Biometrics, 15,
192-218.
Hiendleder S, Mainz K, Plante Y, Lewalski H (1998) Analysis of mitochondrial DNA
indicates that domestic sheep are derived from two different ancestral maternal
sources: no evidence for contributions from urial and argali sheep. Journal of
Heredity, 89, 113-120.
IUCN Species Survival Commission (2000) IUCN red list categories and criteria, version
3.1. Gland, Switzerland.
Joshi MB, Rout PK, Mandal AK, Tyler-Smith C, Singh L, Thangaraj K (2004)
Phylogeography and origin of Indian domestic goats. Molecular Biology and
Evolution, 21, 454-462.
Khatkar MS, Thomson PC, Tammen I, Cavanagh JAL, Nicholas FW, Raadsma HW
(2006) Linkage disequilibrium on chromosome 6 in Australian Holstein-Friesian
cattle. Genetics Selection Evolution, 38, 463-477.
Koenig S, Simianer H (2006) Approaches to the management of inbreeding and
relationship in the German Holstein dairy cattle population. Livestock Science, 103,
40-53.
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular
evolutionary genetics analysis and sequence alignement. Briefings in
Bioinformatics, 5, 150-163.
Li L, Zhang J, Zhu J-Q, et al. (2006) Genetic diversity of nine populations of the black
goat (Capra hircus) in Sichuan, PR China. Zoological Science, 23, 229-234.
Liu RY, Lei CZ, Liu SH, Yang CS (2007) Genetic diversity and origin of Chinese
domestic goats revealed by complete mtDNA D-loop sequence variation. Asian-
Australasian Journal of Animal Sciences, 20, 178-183.

- 169 -
Chapter 5 Are cattle, sheep, and goats endangered species?

Loftus RT, MacHugh DE, Bradley DG, Sharp PM (1994) Evidence for two independent
domestication of cattle. Proceedings of the National Academy of Sciences of the
United States of America, 91, 2757-2761.
Lucy MC (2001) Reproductive loss in high-producing dairy cattle: where will it end?
Journal of Dairy Science, 84, 1277-1293.
Luikart G, Fernández H, Mashkour M, England PR, Taberlet P (2006) Origins and
diffusion of domestic goats inferred from DNA markers: example analyses of
mtDNA, Y chromosomes, and microsatellites. In: Documenting domestication.
New genetic and archaeological paradigms (eds. Zeder MA, Bradley DG,
Emshwiller E, Smith BD), pp. 294-305. University of California Press, Ltd,
Berkeley, CA.
Luikart G, Gielly L, Excoffier L, Vigne JD, Bouvet J, Taberlet P (2001) Multiple maternal
origins and weak phylogeographic structure in domestic goats. Proceedings of the
National Academy of Sciences of the United States of America, 98, 5927-5932.
Maiwashe AN, Blackburn HD (2004) Genetic diversity in and conservation strategy
considerations for Navajo Churro sheep. Journal of Animal Science, 82, 2900-
2905.
Malher X, Beaudeau F, Philipot JM (2006) Effects of sire and dam genotype for complex
vertebral malformation (CVM) on risk of return-to-service in Holstein dairy cows
and heifers. Theriogenology, 65, 1215-1225.
Maudet C, Luikart G, Taberlet P (2002) Genetic diversity and assignment tests among
seven French cattle breeds based on microsatellite DNA analysis. Journal of
Animal Science 80, 942-950.
Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genetical
Research, 23, 23-35.
Meadows JRS, Li K, Kantanen J, et al. (2005) Mitochondrial sequence reveals high levels
of gene flow between breeds of domestic sheep from Asian and Europe. Journal of
Heredity, 96, 494-501.
Miretti MM, Dunner S, Naves M, Contel EP, Ferro JA (2004) Predominant African-
derived mtDNA in Caribbean and Brazilian Creole cattle is also found in Spanish
cattle (Bos taurus). Journal of Heredity, 95, 450-453.
Myers N (1996) Environmental services of biodiversity. Proceedings of the National
Academy of Sciences of the United States of America, 93, 2764-2769.
Nomura T, Honda T, Mukai F (2001) Inbreeding and effective population size of Japanese

- 170 -
Chapter 5 Are cattle, sheep, and goats endangered species?

Black cattle. Journal of Animal Science, 79, 366-370.

Odahara S, Chung HJ, Choi SH, et al. (2006) Mitochondrial DNA diversity of Korean
native goats. Asian-Australasian Journal of Animal Sciences, 19, 482-485.
Pedrosa S, Uzun M, Arranz J-J, Gutiérrez-Gil B, San Primitivo F, Bayón Y (2005)
Evidence of three maternal lineages in near eastern sheep supporting multiple
domestication events. Proceedings of the Royal Society of London Series B, 272,
2211-2217.
Pellecchia M, Negrini R, Colli L, et al. (2007) The mystery of Etruscan origins: novel
clues from Bos taurus mitochondrial DNA. Proceedings of the Royal Society of
London Series B-Biological Sciences, 274, 1175-1179.
Pereira F, Pereira L, Van Asch B, Bradley DG, Amorim A (2005) The mtDNA catalogue
of all Portuguese autochthonous goat (Capra hircus) breeds: high diversity of
female lineages at the western fringe of European distribution. Molecular Ecology,
14, 2313-2318.
Peter C, Bruford M, Perez T, et al. (2007) Genetic diversity and subdivision of 57
European and Middle-Eastern sheep breeds. Animal Genetics, 38,37–44.
Peters J, von den Driesch A, Helmer D (2005) The upper Eurphrates-Tigris basin: cradle
of agro-pastoralism? In: The first steps of animal domestication. New
archaeological approaches (eds. Vigne JD, Peters J, Helmer D), pp. 96-124.
Oxbow Books, Oxford, UK.
Rabasa SL (1950) Genetical reduction of a reproductive unit in relation to the male-female
ratio. Nature, 166, 821-822.
Rogers AR, Jorde LB (1996) Ascertainment bias in estimates of average heterozygosity.
American Journal of Human Genetics, 58, 1033-1041.
Roosen J, Fadlaoui A, Bertaglia M (2005) Economic evaluation for conservation of farm
animal genetic resources. Journal of Animal Breeding and Genetics, 122, 217-228.
Sardina MT, Ballester M, Marmi J, et al. (2006) Phylogenetic analysis of Sicilian goats
reveals a new mtDNA lineage. Animal Genetics, 37, 376-378.
Scherf BD (2000) World watch list for domestic animal diversity (3rd edition). Food and
Agriculture Organization of the United Nations, Rome.
Sørensen AC, Sørensen MK, Berg P (2005) Inbreeding in Danish dairy cattle breeds.
Journal of Dairy Science, 88, 1865-1872.
Soulé ME, Mills LS (1998) Population genetics - No need to isolate genetics. Science,
282, 1658-1659.

- 171 -
Chapter 5 Are cattle, sheep, and goats endangered species?

Sultana S, Mannen H, Tsuji S (2003) Mitochondrial DNA diversity of Pakistani goats.

Animal Genetics, 34, 417-421.
Tapio M, Marzanov N, Ozerov M, et al. (2006) Sheep mitochondrial DNA variation in
European, Caucasian, and Central Asian areas. Molecular Biology and Evolution,
23, 1776-1783.
Tapio M, Tapio I, Grislis Z, et al. (2005) Native breeds demonstrate high contributions to
the molecular variation in northern European sheep. Molecular Ecology, 14, 3951-
3963.
Townsend SJ (2000) Genetic diversity and domestication in sheep (Ovis), PhD thesis,
University of East Anglia.
Troy CS, MacHugh DE, Bailey JF, et al. (2001) Genetic evidence for Near-Eastern origins
of European cattle. Nature, 410, 1088-1091.
Vallejo RL, Li YL, Rogers GW, Ashwell MS (2003) Genetic diversity and background
linkage disequilibrium in the North American Holstein cattle population. Journal
of Dairy Science, 86, 4137-4147.
Vigne JD, Helmer D, Peters J (2005) New archaeozoological approaches to trace the first
steps of animal domestication: general presentation, reflections and proposals. In:
The first steps of animal domestication. New archaeological approaches (eds.
Vigne JD, Peters J, Helmer D), pp. 1-16. Oxbow Books, Oxford.
Vishwanath R (2003) Artificial insemination: the state of the art. Theriogenology, 59, 571-
584.
Weigel KA (2001) Controlling inbreeding in modern breeding programs. Journal of Dairy
Science, 84 (E. Suppl.), E177-E184.
Wood NJ, Phua SH (1996) Variation in the control region sequence of the sheep
mitochondrial genome. Animal Genetics, 271, 25-33.
World Trade Organization (2001) Ministerial Conference, Fourth Session, Doha, 9-14
November 2001.
Zeder MA (2005) A view from the Zagros: new perspectives on livestock domestication in
the Fertile Crescent. In: The first steps of animal domestication. New
archaeological approaches (eds. Vigne JD, Peters J, Helmer D), pp. 125-146.
Oxbow Books, Oxford, UK.
Zeder MA, Emshwiller E, Smith BD, Bradley DG (2006) Documenting domestication:
the intersection of genetics and archaeology. Trends in Genetics, 22, 139-155.
Zeuner FE (1963) A history of domesticated animals. Hutchison, London.

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Discussion and Conclusion
 Discussion, Conclution and Perspective

Discussion and Conclusion

Since the beginning of the domestication, demographic processes, mutations, genetic

drift, local adaptation and selection of breeds have modelled the genetic diversity of
domestic populations. Therefore, understanding the population genetics of the domestic
animals and of their wild progenitors is an essential prerequisite for the comprehension of
the history of domestication, but also for designing conservation genetics programs. This
is especially the case for the goat (Capra hircus) which was one of the first domesticated
ungulates in Fertile Crescent more than 10,000 years ago. Thus, for investigating the
evolutionary history and domestication process of this species, we studied the present
genetic diversity of goat and of its wild progenitor (C. aegagrus).
We first provided a standard method for identifying the current genetic diversity of
the goat at a worldwide scale. Thanks to this method and to a large-scale sampling, we
were able to establish a clear nomenclature of the goat mtDNA haplogroups and also to
assess the pertinence of defining new haplogroups. This survey involved the analysis of
2430 goats mtDNA sequences, including 946 new individuals coming from areas not often
studied until now, especially from the Fertile Crescent. The analysis concerned the first
hyper-variable fragment of the control region of the mtDNA. This fragment is extremely
diverse, as attested by the 1540 haplotypes found out of the 2430 individuals analyzed. We
found a large genetic diversity within 5 of the 6 haplogroups defined. However, the
diversity is mainly distributed among goat haplogroups within the geographical areas. This
weak phylogeographic structure of domestic goat probably results from the ubiquity of the
A haplogroup which is strongly dominating (more than 90% of the individuals) and also
from the broad distribution of the other haplogroups, which might be related to the human
migrations.
But, even with a huge data set (2430 worldwide distributed individuals), it remains
difficult to understand the domestication history by the genetic analysis of domestic goats
on its own. First, it is difficult to estimate accurately if the demographic expansion came
before or after the time of domestication. Second, it remains difficult to identify the
domestication centre(s). A gradient of variability is expected to come out from the
domestication centre(s), but the low phylogeographic structure of goats does not allow
identifying such a pattern. Third, the measurement of the genetic diversity of goat by itself
does not allow testing precisely the occurrence of a bottleneck at the time of
domestication. The study of bezoars together with goats brought new information that

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 Discussion, Conclution and Perspective

allows to reconstitute the history of domestication and to fully understand its process. New
information came from the locations of wild haplotypes close to domestics, from the
comparison between mtDNA and nuclear DNA, and from the comparison of the past
demography of the wilds close to domestics compared to other bezoars. These new data,
based on an extensive sampling (of 487 modern bezoars from 43 localities covering most
of the distribution range) lead to a new two-step scenario for goat domestication. The first
step of this scenario corresponds to an early phase of sustainable management of wild
herds by humans, coming before the effective domestication. During this pre-
domestication phase, some wild flocks of ancient bezoars have undergone a demographic
expansion that is still detectable today. The estimate of parameters characterizing the
demographic history of the populations from the genetic data shows significantly higher
population growth rate at the bezoars bearing haplotypes close to domestic goats.
Following pre-domestication, the second step is the effective domestication consisting in
the capture of bezoars from the managed herds. The current geographic distribution of
bezoars genetically close-to-domestics, encompasses a large area that includes Eastern
Anatolia, the whole Zagros, the Central Iranian Plateau, and Northeastern Iran. This is in
favour of a large-scale phenomenon, both during the pre-domestictaion and the
domestication phases. The domestication of goats has also been a large-scale event at on a
genetic point of view. The combined analysis of mtDNA and nuclear DNA polymorphism,
for bezoars and domestic goats, demonstrated that a large genetic diversity, corresponding
to a large number of mtDNA haplotypes, was captured at the initial step of the effective
domestication. The first domesticated goats were able to capture most of the genetic
diversity of their wild ancestors and clearly, goats do not fit with the bottleneck
domestication paradigm. This scenario is very different from previous models, which call
for restricted domestication centres and population bottlenecks.

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 Discussion, Conclution and Perspective

Perspectives

Fully understanding the evolutionary history of domestic goats would also require the
use of nuclear markers. For example, our study confirmed that more than 77 % of the
mtDNA variation is found within goat breeds and that nearly 25% of the breeds are
composed of at least 2 haplogroups. This is in accordance with the recent fragmentation of
local goat populations into discrete breeds about 200 years ago, under strong selection
pressures on a few phenotypic traits. This structure can be seen on nuclear markers linked
to the selected parts of the genome. This kind of study can be important, especially
because of the critical situation of several breeds. Moreover, sequencing many nuclear
genes would give a huge amount of information that could lead to estimate accurately the
expansion times of bezoars genetically close-to-domestics and goats. Such data would
allow testing the occurrence of a pre-domestication phase, which would involve an
expansion of bezoars before that of goats.
We also propose the study of ancient goat samples from archaeological sites.
Comparing the modern and ancient genetic diversity with different molecular markers can
help determining the differentiation between them, and then can lead to identify the
causative mutations for phenotypic variation. This will allow to trace gene selection and
the spread of economically important alleles during domestication.
Finally, we propose to test if such a large-scale scenario without bottlenecks that we
found in goat is also applicable to other domestic animals. Is the absence of bottlenecks
during the domestication process a prerequisite for a successful and sustainable
domestication?

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Bibliography
 Bibliography

Bibliography

Agyemang K (2005) Trypanotolerant livestock in the context of trypanosomiasis

intervention strategies Food and Agriculture Organization of the United Nations,
Rome.

Ajmone-Marsan P, Negrini R, Crepaldi P, Milanesi E, Gorni C, Valentini A, Cicogna M

(2001) Assessing genetic diversity in Italian goat populations by AFLP markers.
Animal Genetics 32, 281-288.

Ajmone-Marsan P, Valentini A, Cassandro M, Vecchiotti-Antaldi G, Bertoni G, Kuiper

MTR (1997) AFLPTM markers for DNA fingerprinting in cattle. Animal Genetics
28, 418-426.

Alandia Robles E, Gall C, Valle Zárate A (2006) Global gene flow in goats. In: Gene flow
in animal genetic resources: a study on status, impact and trends (eds. Valle
Zárate A, Musavaya K, Schäfer C), pp. 229–240, FAO, GTZ, BMZ.

Alderson L (2001) Foot-and-mouth disease in the United Kingdom 2001; its cause, course,
control and consequences. RBI/EAAP/FAO meeting, Budapest.

Amills M, Capote J, Tomas A, Kelly L, Obexer-Ruff G, Angiolillo A, Sanchez A (2004)

Strong phylogeographic relationships among three goat breeds from the Canary
Islands. Journal of Dairy Research 71, 257-262.

Anderung C, Bouwman A, Persson P, Carretero JM, Ortega AI, Elburg R, Smith C,

Arsuaga JL, Ellegren H, Gotherstrom A (2005) Prehistoric contacts over the Straits
of Gibraltar indicated by genetic analysis of Iberian Bronze Age cattle.
Proceedings of the National Academy of Sciences of the United States of America
102, 8431-8435.

Avise JC (2000) Phylogeography, The history and formation of a species. Cambridge,

Harvard University Press.

Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC
(1987) Intraspecific phylogeography: the mitochondrial DNA bridge between
population genetics and systematics. Annual Review of Ecology, Evolution, and
Systematics 18, 489-522.

Azor PJ, Monteagudo LV, Luque M, Tejedor MT, Rodero E, Sierra I, Herrera M, Rodero
A, Arruga MV (2005) Phylogenetic relationships among Spanish goats breeds.
Animal Genetics 36, 423-425.

- 176 -
 Bibliography

Baker RL, Mwamachi DM, Audho JO, Aduda EO, Thorpe W (1998) Resistance of Galla
and Small East African goats in the sub-humid tropics to gastrointestinal nematode
infections and the peri-parturient rise in faecal egg counts. Veterinary Parasitology
79, 53-64.

Balasse M, Tresset A, Bocherens H, Mariotti A, Vigne J-D (2000) Un abattage "post-

lactation" sur des bovins domestiques Neolithiques. Etude isotopique des restes
osseux du site de Bercy (Paris, France). Anthropozoologica 31, 39-48.

Ball RM, Freeman S, James FC, Bermingham E, Avise JC (1988) Phylogeographic

population structure of Red-winged Blackbirds assessed by mitochondrial DNA.
Proceedings of the National Academy of Sciences of the United States of America
85, 1558-1562.

Beja-Pereira A, Caramelli D, Lalueza-Fox C, Vernesi C, Ferrand N, Casoli A, Goyache F,

Royo LJ, Conti S, Lari M, Triantaphylidis C, Ploumi K, Sineo L, Mallegni F,
Taberlet P, Erhardt G, Sampietro L, Bertranpetit J, Barbujani G, Luikart G,
Bertorelle G (2006) The origin of European cattle: evidence from modern and
ancient DNA. Proceedings of the National Academy of Sciences of the United
States of America 103, 8113-8118.

Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel

sous Windows TM pour la génétique des populations. Laboratoire Génome,
Populations, Interactions, CNRS UMR 5000, Université de Montpellier II,
Montpellier (France).

Benzécri JP (1973) L'analyse des données, 2.L'analyse des correspondances Dunod, Paris.

Boichard D, Maignel L, Verrier E (1996) Analyse généalogique des races bovines laitières
françaises. INRA Productions Animales 9, 323-335.

Bradley DG (2006) Documenting Domestication, Reading Animal Genetic Texts In:

Documenting Domestication: New genetic and archaeological paradigms (eds.
Zeder MA, Bradley DG, Emshwiller E, Smith, BD), pp. 273-278, University of
California Press, Berkeley, USA.

Bradley DG, MacHugh DE, Cunningham P, Loftus R (1996) Mitochondrial diversity and
the origins of African and European cattle. Proceedings of the National Academy
of Sciences of the United States of America 93, 5131-5135.

Bradley DG, Magee DA (2006) Genetics and origins of domestic cattle. In: Documenting
domestication. New genetics and archaeological paradigms (eds. Zeder MA,
Bradley DG, Emshwiller E, Smith BD), pp. 317-328. University of California
Press, Ltd, Berkeley, CA.

- 177 -
 Bibliography

Britton T, Anderson C, Jacquet D, Lundquist S, Bremer K (2007) Estimating divergence

times in large phylogenetic trees. Systematic Biology, in press.

Brown D, Anthony D (1998) Bit wear, horseback riding and the Botai site in Kazakstan.
Journal of Archaeological Science 25, 331-347.
Bruford MW, Bradley DG, Luikart G (2003) DNA markers reveal the complexity of
livestock domestication. Nature Reviews Genetics 3, 900-910.

Bruford MW, Townsend SJ (2006) Mitochondrial DNA diversity in modern sheep:

implications for domestication. In: Documenting domestication. New genetics and
archaeological paradigms (eds. Zeder MA, Bradley DG, Emshwiller E, Smith
BD), pp. 306-316. University of California Press, Ltd, Berkeley, CA.

Cañon J, Garcı´a D, Garcı´a-Atance M, A, Obexer-Ruff G, Lenstra J, A, Ajmone-Marsan

P, Dunner S, Consortium TE (2006) Geographical partitioning of goat diversity in
Europe and the Middle East. Animal Genetics 37, 327–334.

Cappuccio I, Pariset L, Valentini A (2003) Is artificial selection in Italian Holstein Friesian

cattle favouring heterozygotes? Italian Journal of Animal Science 2, 115-117.

Cauvin J (2000) The Birth of the Gods and the Origins of Agriculture. Cambridge Univ
Press, Cambridge, UK.

Chen SY, Su YH, Wu SF, Sha T, Zhang YP (2005) Mitochondrial diversity and
phylogeographic structure of Chinese domestic goats. Molecular Phylogenetics
and Evolution 37, 804-814.

Clutton-Brock J (1999) Domesticated animals from early times. British Museum (Natural
History) and William Heinemann.

Cockett NE, Smit MA, Bidwell CA, Segers K, Hadfield TL, Snowder GD, Georges M,
Charlier C (2005) The callipyge mutation and other genes that affect muscle
hypertrophy in sheep. Genetic Selection and Evolution 37, 65–81.

Columella LIM (circa 60) De re rustica, liber VII II. De ovibus emendis tuendisque.
[Link]

Consultative Group on International Agricultural Research Science Council (2005)

Conservation of Livestock and Fish Genetic Resources Joint report of two studies
commissioned by the CGIAR Science Council.

Cymbron T, Loftus RT, Malheiro MI, Bradley DG (1999) Mitochondrial sequence

variation suggests an African influence in Portuguese cattle. Proceedings of the
Royal Society of London Series B-Biological Sciences 266, 597-603.

- 178 -
 Bibliography

Denver DR, Morris K, Lynch M, Vassilieva LL, Thomas WK (2000) High Direct Estimate
of the Mutation Rate in the Mitochondrial Genome of Caenorhabditis elegans.
Science 289, 2342.
Diamond J (2002) Evolution, consequences and future of plant and animal domestication.
Nature 418, 700-707.

Diamond J, Bellwood P (2003) Farmers and their languages: the first expansions. Science
300, 597-603.

Dobney K, Larson G (2006) Genetics and animal domestication: new windows on a

elusive process. Journal of Zoology 269, 261-271.

Epstein H, Mason IL (1984) Cattle. In: Evolution of domesticated animals (ed. Mason IL),
pp. 6-27. Longman Inc., New York.

Esquinas-Alcazar J (2005) Protecting crop genetic diversity for food security: political,
ethical and technical challenges. Nature Reviews Genetics 6, 946-953.

Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software

package for population genetics data analysis. Evolutionary Bioinformatics Online
1, 47-50.

FAO (1999) The global strategy for the management of farm animal genetic resources.
Executive Brief, Rome.

FAO (2006) DAD-IS (Domestic Animal Diversity Information System).

[Link]

FAO (2007) The state of the world's animal genetic resources for food and agriculture.
COMMISSION ON GENETIC RESOURCES FOR FOOD AND AGRICULTURE,
Rome.

Farnir F, Coppieters W, Arranz JJ, Berzi P, Cambisano N, Grisart B, Karim L, Marcq F,

Moreau L, Mni M, Nezer C, Simon P, Vanmanshoven P, Wagenaar D, Georges M
(2000) Extensive genome-wide linkage disequilibrium in cattle. Genome Research
10, 220-227.

Fernández H, Hugues S, Vigne JD, Helmer D, Hodgins G, Miquel C, Hänni C, Luikart G,

Taberlet P (2006) Divergent mtDNA lineages of goats in an Early Neolithic site,
far from the initial domestication areas. Proceedings of the National Academy of
Sciences of the United States of America 103, 15375-15379.

Fernández H, Taberlet P, Mashkour M, Vigne JD, Luikart G (2005) Assessing the origin
and diffusion of domestic goats using ancient DNA. In: The first steps of animal
domestication. New archaeological approaches (eds. Vigne JD, Peters J, Helmer
D), pp. 50-54. Oxbow Books, Oxford, UK.

- 179 -
 Bibliography

Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics

Cambridge University Press, Cambridge, UK.

Franklin IR (1980) Evolutionary changes in small populations. In: Conservation biology:

an evolutionary-ecological perspective (eds. Soulé ME, Wilcox BA), pp. 135-149.
Sinauer, Sunderland, MA.

Freeman AR, Meghan CM, Machugh DE, Loftus RT, Achukwi MD, Bado A, Sauveroche
B, Bradley DG (2004) Admixture and diversity in West African cattle populations.
Molecular Ecolology 13, 3477–3487.

Fumagalli L, Taberlet P, Favre L, Hausser J (1996) Origin and evolution of homologous

repeated sequences in the mitochondrial DNA control region of shrews. Molecular
Biology and Evolution 13, 31-46.

Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW (1995) An evaluation of

genetic distances for use with microsatellite loci. Genetics 139, 463-471.

Grobet L, Poncelet D, Royo LJ, Brouwers B, Pirottin D, Michaux C, Menissier F, Zanotti

M, Dunner S, Georges M (1998) Molecular definition of an allelic series of
mutations disrupting the myostatin function and causing double-muscling in cattle.
Mammalian Genome 9(3), 210–213.

Guilaine J (2003) De la Vague à la Tombe. La Conquête Néolithique de la Méditerranée

(Le Seuil, Paris).

Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large
phylogenies by maximum likelihood. Systematic Biology 525, 696-704.

Guo J, Du LX, Ma YH, Guan WJ, Li HB, Zhao QJ, Li X, Rao SQ (2005) A novel
maternal lineage revealed in sheep (Ovis aries). Animal Genetics 36, 331-336.

Hall SJG (2004) Livestock biodiversity: genetic resources for the farming of the future.
Oxford, UK. Blackwell Science Ltd.

Hanotte O, Jianlin H (2005) Genetic characterization of livestock populations and its use
in conservation decision making, In: Proceeding of the international workshop:
The role of biotechnology for the characterization and conservation of crop,
forestry, animal and fishery genetic resources, Turin, Italy, pp. 131–136.

Hanotte O, TAWAH CL, BRADLEY DG, OKOMO M, VERJEE Y, OCHIENG J, REGE

JEO (2000) Geographic distribution and frequency of a taurine Bos taurus and an
indicine Bos indicus Y specific allele amongst sub-Saharan African cattle breeds.
Molecular Ecology 9, 387–396.

Harris DR (1996) The origins and spread of agriculture and pastoralism in Eurasia.
Smithsonian Institution Press, Washington D.C.

- 180 -
 Bibliography

Hartl GB, Burger H, Willing R, Suchentrunk F (1990) On the biochemical systematics of

the Caprini and Rupicaprini. Biochemical Systematics and Ecology 18, 175–182.

Hellborg L, Ellegren H (2004) Low levels of nucleotide diversity in mammalian Y

chromosomes. Molecular Biology and Evolution 21, 158–163.
Helmer D, Gourichon L in: Archaeozoology of the Near East VIII, Proc. 4th int. Symp.
Archaeozoology of Southwestern Asia and adjacent areas (eds Vila, E. &
Gourichon, L.). in press (Maison de l’Orient Méditerranéen, Lyon).
Helmer D, Gourichon L, Monchot H, Peters J, Segui MS (2005) Identifying early
domestic cattle from pre-pottery Neolithic sites on teh Middle Eurphrates using
sexual dimorphism. In: The first steps of animal domestication. New
archaeological approaches (eds. Vigne JD, Peters J, Helmer D), pp. 86-95. Oxbow
Books, Oxford, UK.

Henderson CR, Kempthorne O, Searle SR, Von Krosigk CN (1959) Estimation of

environmental and genetic trends from records subject to culling. Biometrics 15,
192-218.

Hiendleder S, Lewalski H, Wassmuth R, Janke A (1998a) The complete mitochondrial

DNA sequence of the domestic sheep (Ovis aries) and comparison with the other
major ovine haplotype. Journal of Molecular Evolution 47, 441-448.

Hiendleder S, Mainz K, Plante Y, Lewalski H (1998b) Analysis of mitochondrial DNA

indicates that domestic sheep are derived from two different ancestral maternal
sources: no evidence for contributions from urial and argali sheep. Journal of
Heredity 89, 113-120.

Ho SYW, Larson G (2006) Molecular clocks: When times are a-changin'. Trends in
Genetics 22, 79-83.

Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular

rate estimates and systematic overestimation of recent divergence times. Molecular
Biology and Evolution 22, 1561-1568.

Ho SYW, Shapiro B, Phillips MJ, Cooper A, Drummond AJ (2007) Evidence for time
dependency of molecular rate estimates. Systematic Biology 56, 515-522.

Hole F (1996) The context of caprine domestication in the Zagros region. In: The origins
and spread of agriculture and pastoralism in Eurasia (ed. Harris DR), pp. 263-
281. Smithsonian Institution Press, Washington D.C.

Hongo H, Meadow RH (2000) Faunal remains from prepottery Neolithic levels at Çayönü,
Southeastern Turkey: a preliminary report focusing on pig (Sus sp.). In: 4th int.
Symp. Archaeozoology of Southwestern Asia and adjacent areas (ASWA; Paris,

- 181 -
 Bibliography

Juin 1998). Groningen: Archaeological Research and Consultancy, Publicaties 32,

121-140.

Horwitz LK (1989) Reassessment of caprovine domestication in the Levantine Neolithic:

old questions, new answers. In: People and culture in change (Proc. 2nd Symp. On
Upper Palaeolithic, Mesolithic and Neolithic of Europe and the Mediterranean
Basin), Part i. British Archaeol. Rep., Int. Ser. (ed. Hershkovitz I), pp. 153-181.

Horwitz LK, Tchernov P, Ducos P, Becker C, von den Driesch A, Martin L, Garrard A
(2000) Animal domestication in the Southern Levant. Paléorient 25, 63-80.

Howell N, Smejkal CB, Mackey DA, Chinnery PF, Turnbull DM, Herrnstadt C (2003)
The Pedigree Rate of Sequence Divergence in the Human mitochondrial Genome:
There Is a Difference Between Phylogenetic and Pedigree Rates. American Journal
of Human Genetics 72, 659–670.

Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees.

Bioinformatics 178, 754-755.

IUCN Species Survival Commission (2000) IUCN red list categories and criteria, version
3.1. Gland, Switzerland.

Jaccard P (1908) Nouvelles recherches sur la distribution florale. Bulletin de la Société

Vaudoise de Sciences Naturelles 44, 223-270.

Jansen T, Forster P, Levine MA, Oelke H, Hurles M, Renfrew C, Weber J, Olek K (2002)
Mitochondrial DNA and the origins of the domestic horse. Proceedings of the
National Academy of Sciences of the United States of America 99, 10905-10910.

Jarne P, Ladoga PJL (1996) Microsatellites, from molecules to populations and back.
Trends in Ecology & Evolution 11, 424-429.

Johnson LN, Kotz S, Kemp AW (1992) Univariate Discrete Distributions, 2nd Edition
John Wiley & Sons, New York.

Joshi MB, Rout PK, Mandal AK, Tyler-Smith C, Singh L, Thangaraj K (2004)
Phylogeography and origin of Indian domestic goats. Molecular Biology and
Evolution 21, 454-462.

Karp A, Ingram D, Isaac P (1997) Molecular tools for screening biodiversity. Kluwer
Academic Publishers, Dordrecht.

Khatkar MS, Thomson PC, Tammen I, Cavanagh JAL, Nicholas FW, Raadsma HW
(2006) Linkage disequilibrium on chromosome 6 in Australian Holstein-Friesian
cattle. Genetics Selection Evolution 38, 463-477.

- 182 -
 Bibliography

Kimura M (1980) A simple method for estimating evolutionary rate of base substitution
through comparative studies of nucleotide sequences. Journal of Molecular
Evolution 16, 111-120.

Koenig S, Simianer H (2006) Approaches to the management of inbreeding and

relationship in the German Holstein dairy cattle population. Livestock Science 103,
40-53.

Koslowski SK (1989-99) Nemrik 9 - Pre Pottery neolithic site in Iraq. Warsaw vol 1-5.

Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of

population parameters. Bioinformatics 22, 768-770.

Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular

evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics
5, 150-163.

Lambert DM, Ritchie PA, Millar CD, Holland B, Drummond AJ, Baroni C (2002) Rates
of Evolution in Ancient DNA from Adélie Penguins. Science 295, 2270.

Larson G, Albarella U, Dobney K, Rowley-Conwy P, Schibler J, Tresset A, Vigne J-D,

Edwards CJ, Schlumbaum A, Dinu A, Bălăçsescu A, Dolman G, Tagliacozzo A,
Manaseryan N, Miracle P, Van Wijngaarden-Bakker L, Masseti M, Bradley DG,
Cooper A (2007) Ancient DNA, pig domestication, and the spread of the Neolithic
into Europe. Proceedings of the National Academy of Sciences of the United States
of America 104 (39), 15276–15281.

Legge AJ (1972) in: Papers in economic prehistory (ed Higgs, E. S.) 119-124 (Cambridge
University Press, Cambridge).

Legge AJ (1996) The beginning of caprine domestication in Southwest Asia. In: The
origins and spread of agriculture and pastoralism in Eurasia (ed. Harris DR), pp.
238-262. Smithsonian Institution Press, Washington D.C.

Li L, Zhang J, Zhu J-Q, Gu S, Sun Q, Zhou G-M, Fu C-X, Li Q, Chen L-Y, Li D-X, Liu
S-J, Yang Z-R (2006) Genetic diversity of nine populations of the black goat
(Capra hircus) in Sichuan, PR China. Zoological Science 23, 229-234.

Liu RY, Lei CZ, Liu SH, Yang CS (2007) Genetic diversity and origin of Chinese
domestic goats revealed by complete mtDNA D-loop sequence variation. Asian-
Australasian Journal of Animal Sciences 20, 178-183.

Loftus RT, ERTUGRUL O, HARBA AH, EL-BARODY MAA, MACHUGH DE, PARK
SDE, BRADLEY DG (1999) A microsatellite survey of cattle from a centre of
origin: the Near East. Molecular Ecology 8, 2015–2022.

- 183 -
 Bibliography

Loftus RT, MacHugh DE, Bradley DG, Sharp PM (1994) Evidence for two independent
domestication of cattle. Proceedings of the National Academy of Sciences of the
United States of America 91, 2757-2761.

Lucy MC (2001) Reproductive loss in high-producing dairy cattle: where will it end?
Journal of Dairy Science 84, 1277-1293.

Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of
population genomics: from genotyping to genome typing. Nature Reviews Genetics
4, 981-994.

Luikart G, Fernández H, Mashkour M, England PR, Taberlet P (2006) Origins and

diffusion of domestic goats inferred from DNA markers: example analyses of
mtDNA, Y chromosomes, and microsatellites. In: Documenting Domestication:
New genetic and archaeological paradigms (eds. Zeder MA, Bradley DG,
Emshwiller E, Smith BD), pp. 294-305. University of California Press, Berkeley,
USA.

Luikart G, Gielly L, Excoffier L, Vigne J-D, Bouvet J, Taberlet P (2001) Multiple

maternal origins and weak phylogeographic structure in domestic goats.
Proceedings of the National Academy of Sciences of the United States of America
98, 5927-5932.

MacHugh DE, Bradley DG (2001) Livestock genetic origins: goats buck the trend.
Proceedings of the National Academy of Sciences of the United States of America
98, 5382-5384.

MacHugh DE, Shriver MD, Loftus RT, Cunningham P, Bradley DG (1997) Microsatellite
DNA variation and the evolution, domestication and phylogeography of taurine
and Zebu cattle (Bos taurus and Bos indicus). Genetics 146, 1071-1086.

Maiwashe AN, Blackburn HD (2004) Genetic diversity in and conservation strategy

considerations for Navajo Churro sheep. Journal of Animal Science 82, 2900-2905.

Malher X, Beaudeau F, Philipot JM (2006) Effects of sire and dam genotype for complex
vertebral malformation (CVM) on risk of return-to-service in Holstein dairy cows
and heifers. Theriogenology 65, 1215-1225.

Manceau V, Crampe J-P, Boursot P, Taberlet P (1999b) Identification of evolutionary

significant units in the Spanish wild goat Capra pyrenaica (Mammalia,
Artiodactyla). Animal Conservation 2, 33-39.

Manceau V, Despres L, Bouvet J, Taberlet P (1999a) Systematics of the genus Capra

inferred from mitochondrial DNA sequence data. Molecular Phylogenetics and
Evolution 13, 504-510.

- 184 -
 Bibliography

Mannen H, Kohno M, Nagata Y, Tsuji S, Bradley DG, Yeo JS, Nyamsamba D, Zagdsuren
Y, Yokohama M, Nomura K, Amanof T (2004) Independent mitochondrial origin
and historical genetic differentiation in North Eastern Asian cattle. Molecular
Phylogenetics and Evolution 32, 539–544.

Mannen H, Nagata Y, Tsuji S (2001) Mitochondrial DNA reveal that domestic goat
(Capra hircus) are genetically affected by two subspecies of bezoar (Capra
aegagrus). Biochemical Genetics 39, 145-154.

Mashkour M (2006) In: The Origins of State Organizations in Prehistoric Highland Fars,
Excavations atT all-e Bakun (ed Alizadeh, A.),pp. 101-105. Oriental Institut
Publications 128, Chicago. Illinois.

Maudet C, Luikart G, Taberlet P (2002) Genetic diversity and assignment tests among
seven French cattle breeds based on microsatellite DNA analysis. Journal of
Animal Science 80, 942-950.

Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favourable gene. Genetical
Research 23, 23-35.

Meadow RH (1981) Early animal domestication in South Asia: a first report of the faunal
remains from Mehrgarh, Pakistan. In: Härtel H; ed., South Asian Archaeology
1979., 143-179.

Meadow RH (1984) Notes on the faunal remains from Mehrgarh, with a focus on cattle
(Bos). In: B. Allchin ed., South Asian Archaeology 1981, 34-40.

Meadow RH (1996) The origins ans spread of agriculture and pastoralism in northwestern
South Asia. In: The origins and spread of agriculture and pastoralism in Eurasia
(ed. Harris DR), pp. 390-412. Smithsonian Institution Press, Washington D.C.

Meadows JRS, Cemal I, Karaca O, Gootwine E, Kijas JW (2007) Five ovine

mitochondrial lineages identified from sheep breeds of the near east. Genetics 175,
1371-1379.

Meadows JRS, Hawken RJ, Kijas JW (2004) Nucleotide diversity on the ovine Y
chromosome. Animal Genetics 35, 379–385.

Meadows JRS, Li K, Kantanen J, Tapio M, Sipos W, Pardeshi V, Gupta V, Calvo JH,

Whan V, Norris B, Kijas JW (2005) Mitochondrial sequence reveals high levels of
gene flow between breeds of domestic sheep from Asian and Europe. Journal of
Heredity 96, 494-501.

Mignon-Grasteau S, Boissy A, Bouix J, Faure J-M, Fisher AD, Hinch GN, Jensen P, Le
Neindre P, Mormède P, Prunet P, Vandeputte M, Beaumont C (2005) Genetics of

- 185 -
 Bibliography

adaptation and domestication in livestock. Livestock Production Science 93(1), 3–

14.

Miller MP (1999) MANTEL-STRUCT: A program for the detection of population

structure via Mantel tests. Journal of Heredity 90, 258-259.

Miretti MM, Dunner S, Naves M, Contel EP, Ferro JA (2004) Predominant African-
derived mtDNA in Caribbean and Brazilian Creole cattle is also found in Spanish
cattle (Bos taurus). Journal of Heredity 95, 450-453.

Moore AMT, Legge AJ, Hillman GC (2000) Village on the Euphrates. USA: Oxford
University Press.

Moritz C (1994) Defining "evolutionarily significant units" for conservation. Trends in

Ecology and Evolution, 9, 373-375.

Mueller UG, Wolfenbarger LL (1999) AFLP genotyping and fingerprinting. Trends in

Ecology & Evolution 14, 389-394.

Myers N (1996) Environmental services of biodiversity. Proceedings of the National

Academy of Sciences of the United States of America 93, 2764-2769.

Naderi S, Rezaei H-R, Taberlet P, Zundel S, Rafat SA, Naghash H-R, Abo-Shehada M,
El-Barody MAA, Ertugrul O, Pompanon F, Econogene Consortium (2007) Large-
scale mitochondrial DNA analysis of the domestic goat reveals six maternal
lineages with high haplotype diversity. PLoS ONE 10, e1012.

Naderi S, Rezaei HR, Pompanon F, Blum MGB, Negrini R, Naghash HR, Balkız Ö,
Mashkour M, Gaggiotti O, Ajmone-Marsan P, Kence A, Vigne JD, Taberlet P (In
Prep.) Genetic evidence for a large scale domestication in goats.

Nei M (1987) Molecular evolutionary genetics Columbia University Press, New York,
NY.

Nomura T, Honda T, Mukai F (2001) Inbreeding and effective population size of Japanese
Black cattle. Journal of Animal Science 79, 366-370.

Odahara S, Chung HJ, Choi SH, Yu SL, Sasazaki S, Mannen H, Park CS, Lee JH (2006)
Mitochondrial DNA diversity of Korean native goats. Asian-Australasian Journal
of Animal Sciences 19, 482-485.

Pääbo S (1999) Neolithic genetic engineering. Nature 398, 194-195.

Pariset L, Cappuccio I, Ajmone Marsan P, Dunner S, Luikart G, Obexer-Ruff G, Peter C,

Marletta D, Pilla F, Valentini A, Consortium TE (2006) Assessment of population
structure by single nucleotide polymorphisms (SNPs) in goat breeds. Journal of
Chromatography B.

- 186 -
 Bibliography

Parma P, Feligini M, Greeppi G, Enne G (2003) The complete nucleotide sequence of goat
(Capra hircus) mitochondrial genome. Goat mitochondrial genome. DNA Seqence
14, 199-203.

Pedrosa S, Uzun M, Arranz J-J, Gutiérrez-Gil B, San Primitivo F, Bayón Y (2005)

Evidence of three maternal lineages in near eastern sheep supporting multiple
domestication events. Proceedings of the Royal Society of London Series B 272,
2211-2217.

Pellecchia M, Negrini R, Colli L, Patrini M, Milanesi E, Achilli A, Bertorelle G, Cavalli-

Sforza LL, Piazza A, Torroni A, Ajmone-Marsan P (2007) The mystery of
Etruscan origins: novel clues from Bos taurus mitochondrial DNA. Proceedings of
the Royal Society of London Series B-Biological Sciences 274, 1175-1179.

Pereira F, Pereira L, Van Asch B, Bradley DG, Amorim A (2005) The mtDNA catalogue
of all Portuguese autochthonous goat (Capra hircus) breeds: high diversity of
female lineages at the western fringe of European distribution. Molecular Ecology
14, 2313-2318.

Peter C, Bruford M, Perez T, Dalamitra S, Hewitt G, Erhardt G, Consortium TE (2007)

Genetic diversity and subdivision of 57 European and Middle-Eastern sheep
breeds. Animal Genetics. 38, 37–44.

Peters J, Helmer D, von den Driesch A, Saña-Segui M (1999) Early animal husbandry in
the Northern Levant. Paléorient 25, 27-48.

Peters J, von den Driesch A, Helmer D (2005) The upper Eurphrates-Tigris basin: cradle
of agro-pastoralism? In: The first steps of animal domestication. New
archaeological approaches (eds. Vigne JD, Peters J, Helmer D), pp. 96-124.
Oxbow Books, Oxford, UK.

Pidancier N, Jordan S, Luikart G, Taberlet P (2006) Evolutionary history of the genus

Capra (Mammalia, Artiodactyla): discordance between mitochondrial DNA and
Y-chromosome phylogenies. Molecular Phylogenetics and Evolution 40, 739-749.

Pilgrim GE (1947) The evolution of the buffaloes, oxen, sheep and goats. J. Linn. Soc.
(Zool) 41, 272–286.

Poland M, Hammond-Tooke D, Leigh V (2003) The abundant herds: a celebration of the

cattle of the Zulu people. Vlaeberg, South Africa. Fernwood Press.

Porter V (1996) Goats of the world. Farming Press, Ipswich, UK.

Posada D, Crandall K (1998) Modeltest: testing the model of DNA substitution.

Bioinformatics 14, 817-818.

Pringle H (1998) Reading the signs of ancient animal domestication. Science 282, 1448.

- 187 -
 Bibliography

Queller DC, Strassmann JE, Hughes CR (1993) Microsatellites and kinship. Trends in
Ecology & Evolution 8, 285-288.

Questiau S, Eybert MC, Taberlet P (1999a) Amplified fragment length polymorphism

(AFLP) markers reveal extra-pair parentage in a bird species: the bluethroat
(Luscinia svecica). Molecular Ecology 8, 1331-1339.

Questiau S, Gielly L, Clouet M, Taberlet P (1999b) Phylogeographic evidence of gene

flow among Common Crossbill populations at the continental level (Loxia
curvirostra, Aves, Fringillidae). Heredity 83, 196-205.

Rabasa SL (1950) Genetical reduction of a reproductive unit in relation to the male-female

ratio. Nature 166, 821-822.

Randi E, Fusco G, Lorenzini R, Toso S, Tosi G (1990) Allozyme divergence and

phylogenetic relationships among Capra, Ovis and Rupicapra (Artyodactyla,
Bovidae). Heredity 67, 281-286.

Rogers A, Harpending H (1992) Population growth makes waves in the distribution of

pairwise genetic differences. Molecular Biology and Evolution 9, 552-569.

Rogers AR, Jorde LB (1996) Ascertainment bias in estimates of average heterozygosity.

American Journal of Human Genetics 58, 1033-1041.

Roosen J, Fadlaoui A, Bertaglia M (2005) Economic evaluation for conservation of farm

animal genetic resources. Journal of Animal Breeding and Genetics 122, 217-228.

Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies.

Trends in Ecology and Evolution, 1, 9-10.

Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing
phylogenetic trees. Molecular Biology and Evolution 4, 406-425.

Salamini F, Özkan H, Brandolini A, Schäfer-Pregl R, Martin W (2002) Genetics and

geography of wild cereal domestication in the near east. Nature Reviews Genetics
3, 429–441.

Saña Seguí M (1999) Arqueología de la domesticaión animal. La gestión de los recursos

animales en Tell Halula (Valle del Éufrates-Siria) del 8.800 al 7.000 BP. Treballs
d’Arqueologia del Pròxim Orient 1. Barcelona, Universitat Autònoma de
Barcelona.

Sardina MT, Ballester M, Marmi J, Finocchiaro R, van Kaam J, Portolano B, Folch JM

(2006) Phylogenetic analysis of Sicilian goats reveals a new mtDNA lineage.
Animal Genetics 37, 376-378.

- 188 -
 Bibliography

Schaller GB (1977) Mountain monarchs: Wild Sheep and Goats of the Himalaya.
University of Chicago Press, Chicago.

Scherf BD (2000) World watch list for domestic animal diversity (3rd edition) Food and
Agriculture Organization of the United Nations, Rome, [Link]

Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the

distribution of pairwise differences when the mutation rates vary among sites:
application to human mitochondrial DNA. Genetics 152, 1079-1089.

Scribner KT, Chesser RK (2001) Group-structured genetic models in analysis of the

population and behavioral ecology of poikilothermic vertebrates. Journal of
Heredity 92, 180-189.

Shackleton DM (1997) Wild sheep and goats and their relatives. Status survey and
conservation action plan for Caprinae IUCN, Gland, Switzerland.

Sørensen AC, Sørensen MK, Berg P (2005) Inbreeding in Danish dairy cattle breeds.
Journal of Dairy Science 88, 1865-1872.

Soulé ME, Mills LS (1998) Population genetics - No need to isolate genetics. Science 282,
1658-1659.

Sultana S, Mannen H, Tsuji S (2003) Mitochondrial DNA diversity of Pakistani goats.

Animal Genetics 34, 417-421.

Sunnucks P (2000) Efficient genetic markers for population biology: single locus and
yielding genealogies. Trends in Ecology & Evolution 15, sous presse.

Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (*and other

methods), Version 4. Sinauer Associates, Sunderland, Massachusetts.

Symondson WO (2002) Molecular identification of prey in predator diets. Molecular

Ecology 11, 627-641.

Taberlet P, Valentini A, Rezaei HR, Naderi S, Pompanon F, Negrini R, Ajmone-Marsan P

(2007) Are cattle, sheep, and goats endangered species? Molecular Ecology, in
press.

Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you
leap. Trends in Ecology and Evolution 14, 321-325.

Takada T, Kikkawa Y, Yonekawa H, Kawakami S, Amano T (1997) Bezoar (Capra

aegagrus) is a matriarchal candidate for ancestor of domestic goat (Capra hircus):
evidence from the mitochondrial DNA diversity. Biochemical Genetics 35, 315-
326.

- 189 -
 Bibliography

Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the

control region of mitochondrial DNA in humans and chimpanzees. Molecular
Biology and Evolution 10, 512-526.

Tapio M, Marzanov N, Ozerov M, Cinkulov M, Gonzarenko G, Kiselyova T, Murawski

M, Viinalass H, Kantanen J (2006) Sheep mitochondrial DNA variation in
European, Caucasian, and Central Asian areas. Molecular Biology and Evolution
23, 1776-1783.

Tapio M, Tapio I, Grislis Z, Holm LE, Jeppsson S, Kantanen J, Miceikiene I, Olsaker I,

Viinalass H, Eythorsdottir E (2005) Native breeds demonstrate high contributions
to the molecular variation in northern European sheep. Molecular Ecology 14,
3951-3963.

Townsend SJ (2000) Genetic diversity and domestication in sheep (Ovis), University of

East Anglia.

Troy CS, MacHugh DE, Bailey JF, Magee DA, Loftus RT, Cunningham P, Chamberlain
AT, Sykes BC, Bradley DG (2001) Genetic evidence for Near-Eastern origins of
European cattle. Nature 410, 1088-1091.

Tuñon M, J, Gonzalez P, Vallejo M (1989) Genetic relationships between 14 native

spanish breeds of goat. Animal Genetics 20, 205-212.

Uerpmann H-P (1987) The ancient distribution of Ungulate Mammals in the Middle East.
Dr Ludwig Reichert Verlag, Wiesbaden.

Vallejo RL, Li YL, Rogers GW, Ashwell MS (2003) Genetic diversity and background
linkage disequilibrium in the North American Holstein cattle population. Journal
of Dairy Science 86, 4137-4147.

Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified

fragment length polymorphism (AFLP) markers show indication of size homoplasy
and of a relationship between degree of homoplasy and fragment size. Molecular
Ecology 11, 139-151.

Vernesi C, Pecchiolo E, Caramelli D, Tiedemann R, Randi E, Bertorelle G (2002) The

genetic structure of natural and reintroduced roe deer (Capreolus capreolus)
populations in the Alps and central Italy, with reference to the mitochondrial DNA
phylogeography of Europe. Molecular Ecology 11, 1285-1297.

Vigne JD, Buitenhuis H (1999) Les premiers pas de la domestication animale à l’Ouest de
l’Euphrate: Chypre et l’Anatolie centrale. Paléorient 25, 2, 49-62.

- 190 -
 Bibliography

Vigne JD, Carrère I, Guilaine J (2003) Unstable status of early domestic ungulates in the
near east: the example of Shillourokambos (Cyprus, IX-VIII millenia cal. BC). In:
Le Néolithique de Chypre (eds. Guilaine J, Le Brun A), pp. 239-251.

Vigne JD, Carrère I, Saliège JF, Person A, Bocherens H, Guilaine J, Briois F (2000)
Predomestic cattle, sheep, goat and pig duing the late 9th and 8th millenium cal.
BP on Cyprus: preliminary results of Shillourokambos (Perkklisha, Limassol). In:
Archaeozoology of the Near East IV, Proc. 4th int. Symp. Archaeozoology of
Southwestern Asia and adjacent areas (ASWA; Paris, June 1998) (eds. Mashkour
M, Choyke AM, Buitenhuis H, Poplin F), pp. 52-75. Archaeological Research and
Consultancy, Groningen.

Vigne JD, Helmer D, Peters J (2005a) New archaeozoological approaches to trace the first
steps of animal domestication: general presentation, reflections and proposals. In:
The first steps of animal domestication. New archaeological approaches (eds.
Vigne JD, Peters J, Helmer D), pp. 1-16. Oxbow Books, Oxford, UK.

Vigne JD, Peters J, Helmer D (2005b) The first steps of animal domestication. New
archaeological approaches Oxbow Books, Oxford, UK.

Vishwanath R (2003) Artificial insemination: the state of the art. Theriogenology 59, 571-
584.

Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J,

Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA
fingerprinting. NAR 23, 4407-4414.

Weigel KA (2001) Controlling inbreeding in modern breeding programs. Journal of Dairy

Science 84 (E. Suppl.), E177-E184.

Wood NJ, Phua SH (1996) Variation in the control region sequence of the sheep
mitochondrial genome. Animal Genetics 271, 25-33.

World Trade Organization (2001) Ministerial Conference, Fourth Session, Doha, 9-14
November 2001.

Xuebin Q, Jianlin H, Lkhagva B, Chekarova I, Badamdorj D, Rege JEO, Hanotte O (2005)

Genetic diversity and differentiation of Mongolian and Russian yak populations.
Journal of Animal Breeding and Genetics 122, 117-126.

Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum

likelihood. CABIOS. 13, 555-556.

Zeder MA, Hesse B (2000) The initial domestication of goats (Capra hircus) in the Zagros
Mountains 10,000 years ago. Sciences 287, 2254-2257.

- 191 -
 Bibliography

Zeder MA (2001) A metrical analysis of a collection of modern goats (Capra hircus

aegagrus and C. h. hircus) from Iran and Iraq: Implications for the study of caprine
domestication. Journal of Archaeological Science 28, 61-79.

Zeder MA (2005) A view from the Zagros: new perspectives on livestock domestication in
the Fertile Crescent. In: The first steps of animal domestication. New
archaeological approaches (eds. Vigne JD, Peters J, Helmer D), pp. 125-146.
Oxbow Books, Oxford, UK.

Zeder MA, Emshwiller E, Smith BD, Bradley DG (2006) Documenting domestication: the
intersection of genetics and archaeology. Trends in Genetics 22, 139-155.

Zeder MA, Bradley DG, Emshwiller E, Smith BD (2006a) Documenting domestication.

In: Documenting Domestication: New genetic and archaeological paradigms (eds.
Zeder MA, Bradley DG, Emshwiller E, Smith, BD), pp. 1-12, University of
California Press, Berkeley, USA.

Zeder MA (2006b) Archaeological Approaches to Documenting Animal Domestication.

In: Documenting Domestication: New genetic and archaeological paradigms (eds.
Zeder MA, Bradley DG, Emshwiller E, Smith, BD), pp. 171-180, University of
California Press, Berkeley, USA.

Zeder MA (2006c) A Critical Assessment of Markers of Initial Domestication in Goats

(Capra hircus). In: Documenting Domestication: New genetic and archaeological
paradigms (eds. Zeder MA, Bradley DG, Emshwiller E, Smith, BD), pp. 181-208,
University of California Press, Berkeley, USA.

Zeuner FE (1963) A history of domesticated animals Hutchison, London.

Zhang FF, Jiang ZG (2006) Mitochondrial phylogeography and genetic diversity of

Tibetan gazelle (Procapra picticaudata): Implications for conservation. Molecular
Phylogenetics and Evolution 41, 313-321.

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Annex

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Review of archaeozoological data for the earliest goat domestication

based on Marjan Mashkour and Jean-Denis Vigne studies

The earliest archaeozoological evidences of goat domestication are located in Eastern

Anatolia (high valleys of the Euphrates and Tigris rivers) and in the Central Zagros
mountains (Figure 4.2a). Domestication in the first one occurred five to ten centuries
earlier than in the second one (Figure A1). Archaeology is still unable to tell wether the
Zagros center of goat domestication has been influenced by the Anatolian center or if it
emerged by itself, but it clearly attests important cultural differences between the two
regions (Aurenche & Kozlowski 1999; Cauvin 2000), which suggest weak to no cultural
exchanges between them before the end of the prepottery Neolithic.
A third, but much younger center for goat domestication, is currently accepted for the
eastern footlands of the Balutchistan mountains (Pakistan), at the western boundary of the
Lower Indus plain. There, the long stratigraphy of the site Mehrgarh suggested
management/domestication of goats as early as the earliest pre-pottery Neolithic phase of
the site, ca. 8200-7500 cal. B.P., perhaps a bit before sheep and cattle domestication
(Meadow 1979; Meadow 1981; Meadow 1996).

Eastern Anatolian area

In the Eastern Anatolian area, archaeology detected five main steps in the early
neolithisation process:
- Natufian-Khiamian periods (14,000-11,000 cal. B.P.): like they did in the Southern
Levant (Bar-Yosef & Valla 1991; Valla 2000), some of the human groups of Eastern
Anatolia became sedentary, in small villages with round houses made out of stone and
mud (Cauvin 2000). These small groups of hunters-gatherers achieved their sedentary
lifeway by exploiting a broad spectrum of plants and animals. According to
archaeozoological data from sites such as Mureybeth, large game was mainly
composed of gazelle (Gazella subgutturosa), wild ass (Equus hemionus), aurochs (Bos
primigenius) and, in the highlands, wild sheep (Ovis orientalis) and wild goat (Capra
aegagrus) (Cauvin et al. 1998; Gourichon 2004).
- Pre-Pottery Neolithic A (PPNA) and beginning of the early Pre-Pottery Neolithic B
(PPNB) periods (11,000-10,500 cal. B.P.): villages are much larger and quadrangular
stone houses are organised around large common semi-buried round houses (e. g. Jerf

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El Ahmar, Stordeur 2000). Large collective sites with monumental art such as Göbekli
(Schmidt 2002; Peters & Schmidt 2004) indicate high level of social organisation.
These well-organised villagers practiced predomestic agriculture (Tanno & Willcox
2005). They were however still hunters in a similar way as during the previous period
(Peters et al. 2005), though Rosenberg et al. (1995) claimed a questionable PPNA
sheep, goat and pig management at Hallan Çemi.
- In the course of the early PPNB, ca. 10,500 cal. B.P.: Peters et al. (Peters et al. 2005)
detected clear changes in the culling strategy and slight decrease of size for both sheep
and goat in the earliest layers at Nevalı Çori, a large prepottery village in the upper
Euphrates valley. This is the earliest known evidence of goat domestication in the
world. It is however possible that predomestic or early domestic goat have existed on
other sites of the same area, such as Çayönü, where archaeological data strongly
suggested that sheep, goat, pig and cattle domestication begun during the phase dated to
ca. 9200-9100 cal. B.P. (“Grill Building” phase) but where Hongo and Meadow (2000)
also noticed an increase of the importance of caprines in the diet a bit earlier, ca. 9300-
9200 cal. B.P.
- Starting from the end of the early PPNB and during the Middle PPNB (10,300-9600
cal. B.P.), villages get larger and much well organised, sometimes with very well
standardised house organisations (i.e. Halula, Molist Montaña 1991). Goat bones were
found in numerous of them, out of the natural distribution area of the bezoar, testifying
frequent transfers of small flocks of managed / domestic animals. The Cypriot site of
Shillourokambos gave both the earliest and the most distant evidence of these transfers:
goat has no native ancestor on the island and goat bones have been found in well
isolated layers or deep wells dated to 10,400-10,200 cal. B.P. (Vigne et al. 2000);
however, these goats rapidly ferralized and, between 10,000 and 9,500 cal. B.P., they
were mostly hunted by the villagers of Shillourokambos, who however husbanded
sheep, pig, and probably cattle (Vigne et al. 2003). Approximately at the same date,
goat bones are also found at Aswad (near Damascus) in a plain area where wild goats
probably did not live; they are interpreted as resulting from the transfer of early
domestic goat from Anatolia (Helmer & Gourichon. in press). Starting from ca. 9,800-
9,700 cal. B.P., domestic goat are found at two other large Middle PPNB sites out of
the original area located in the Middle Euphrates valley: Halula (Saña Seguí 1999) and
Abu Hureyra ( Legge 1996; Moore et al. 2000). It is also present more westerly, at
Aşıklı (Central Anatolia; Vigne & Buitenhuis 1999), and more easterly, at Nemrik

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(Northern Iraq, Koslowski 1989-99). In these two last sites however, local wild bezoar
pre-existed, and the question of weather they were locally domesticated or transferred
from other domestication center(s) remains open (orange squares on Figure 4.2a). All
through this period, hunting continued to provide the main part of the meat subsistence,
which leads Helmer and Vigne (in press) to speak of stock breeding cultivators-hunters.
Size decrease and bone modifications due to domestication are undetectable
(Shillourokambos; Vigne et al. 2000, Vigne et al. 2003) or weak (Saña Seguí 1999), so
that they can only result from hormonal modifications due to stock keeping (Zohary
1998), without any clear and deliberate oriented human selection (Helmer and Vigne, in
press; Vigne, in press).
- Starting from the Late PPNB (ca.9500 cal. B.P.), Neolithic villages still grew in size
and organisation. Domesticates then became the most important part of the meat
(Helmer & Vigne, in press). In the same time, important morphological modifications
appeared, which should result from oriented human selective pressures (Zohary 1998).
For goats, this is the time of the first very twisted male and very reduced female
horncores (Clutton-Brock 1981).

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Figure A1. Proposal for a chronological succession of the different phases of goat
domestication in the two main cradles of domestication, Eastern Anatolia (left) and Zagros
(right). Evidences of effective domestication appeared slightly later in the second one.
Vertical segments summarize, for the sites mentioned in Figure 4.2A, the dates of the
earliest evidence of local goat domestication (red), the dates of either local domestication
or transfer of goats (orange) and the dates of earliest appearance out of the original area of
the bezoar (yellow) PPNA: Pre-Pottery Neolithic A , PPNB: Pre-Pottery Neolithic B.

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Iranian Plateau

Contrary to Eastern Anatolia, domestication process remains puzzled on the Iranian

Plateau, certainly due to the scarcity of archaeozoological studies. The Easter fringe of the
Mesopotamian valleys, the Zagros mountains and specifically their central region were
suspected as critical places for the history of ungulates domestication (Braidwood 1961;
Perkins 1961; Perkins 1964; Hole & Flannery 1969). Early goat domestication, more
specifically, was documented by key archaeological sites of the central Zagros, in the
Kermanshah region (Bökönyi 1977; Hesse 1978; Uerpmann 1979; Bar-Yosef & Meadow
1995).
However, M. Zeder (Zeder 1999; Zeder 2000; Zeder 2001; Zeder 2005; Zeder et al.
2006) recently reinvestigated this question in the Zagros using previously studied
archaeozoological Middle Paleolithic to the Neolithic collections, by the way of metrical
and demographic studies and of radiocarbon dating. Analyzing modern bezoars and goats
of the Zagros, she questioned the correlation between domestication and size decrease, and
strengthened the necessity of first relying on demographic profiles for detecting early
domestication. She evidenced early domestication without any size modification in the
central Zagros, at Ganj Dareh, dating to 9,900-9,700 cal. B.P., then at Tapeh Guran
(9,500-9,200 cal. B.P.), two pre-pottery Neolithic sites. She also evidenced early
transportation of non-modified domestic goat to the western Zagros lowlands, at Ali Kosh,
dating to ca. 9,000 cal. B.P.
More recently, new evidence came from animal bone assemblages in central and
southern Zagros (namely Tal-i-Mushki, Fars, 8,000-8,500 cal. B.P., Mashkour et al. 2006)
and in northeastern Iran, farther to the East. There, in southeastern Alborz, the prepottery
Neolithic western mount at Sang-e-Caxmaq (near Shahroud, Masuda 1974) (near
Shahroud, Masuda 1974), has been dated to [9059-8711] cal. B.P. (UB-7157: 7997±42
B.P., level 4) and to [9047-8699] cal. B.P. (UB-7158: 7971±42 B.P., level 1; Mashkour &
Vigne, unpublished data). Preliminary metric analyses of bones evidenced a small size
with reference to early Holocene bezoar at Asiab (dated to 11,000-10,000 cal. B.P.; Zeder
2005), and early goats at Ganj Dareh (Figure A2). We can conclude that the size of the
goat at Sang-e-Caxmaq was much smaller as the size of the wild bezoar which lived in this
area at that time, because the latter should have themselves been larger than the wild goats
of the Zagros (lower altitude and latitude). In addition, the size of the Sang-e-Caxmaq’s

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goats is very similar to the one of the fully domestic goats at Sarab (dated to 9,000-8,000
cal. B.P.; Zeder 2005). Either due to a very high proportion of adult females or to a strong
size decrease with reference to the wild, the small size of goats at Sang-e-Caxmaq clearly
evidence domestication. These preliminary data indicate that goat domestication in this
area, i.e. ca. 1000 km eastern far from the Zagros center of goat pre-domestication, begun
less than 500 years later than in the Zagros area. This is a very early date with reference to
Ali Kosh, where domestic goats are attested approximately at the same dates as at Sang-e-
Caxmaq, but which is located much nearer from the Zagros domestication center. Whether
the birth of goat domestication in the Sang-e-Caxmaq area resulted from a rapid spread of
domestic goat from the Zagros toward the East or from an independent domestication
event of local bezoars remains an open question for archaeologists.

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 Annex

Figure A2. Log size index of the Sang-e-Caxmaq goat compared to those at three
archaeological sites in the Central Zagros.

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 Annex

References

A1. O. Aurenche, S. K. Kozlowski, La naissance du Néolithique au Proche-Orient

(Errance, Paris, 1999), pp. 256.

A2. J. Cauvin, The Birth of the Gods and the Beginnings of Agriculture (Cambridge

University Press, Cambridge U.K., 2000).

A3. R. H. Meadow, in South Asian Archaeology 1979 H. Härtel Ed. (Dietrich Reimer

Verlag, Berlin, 1981) p. 143-179.

A4. R. H. Meadow, in South Asian Archaeology 1981 B. Allchin Ed. (Cambridge Univ.

press, Cambridge, London, New York, New Rochelle, Melbourne, Sydney, 1984)

pp. 34-40.

A5. R. H. Meadow, in The origins and spread of agriculture and pastoralism in Eurasia

D. R. Harris Ed. (Smithsonian Inst, Washington, 1996) pp. 390-412.

A6. O. Bar-Yosef, F. Valla, The Natufian culture in the Levant (Ann Arbor Int.

monograph in Prehist., Ann Arbor, 1991).

A7. F. Valla, in Premiers paysans du monde J. Guilaine Ed. (Errance, Paris, 2000) pp.

11-30

A8. J. Cauvin, M.-C. Cauvin, D. Helmer, G. Willcox, Paléorient 23, 51 (1998).

A9. L. Gourichon, Faune et saisonnalité : l’organisation temporelle des activités de

subsistance dans l’Epipaléolithique et le Néolithique précéramique du Levant nord

(Syrie) (Thèse Doc. Université Lumière – Lyon 2, 2004).

A10. D. Stordeur, M. Brenet, G. Der Aprahamian, J.-C. Roux, Paléorient 26, 29 (2000).

A11. K. Schmidt, Neo-Lithics 2, 8 (2002.).

A12. J. Peters, K. Schmidt, Anthropozoologica 39, 1, 179 (2004).

A13. K. Tanno, G. Willcox, Science 311, 1886 (2005).

- 201 -
 Annex

A14. J. Peters, A. von den Driesch, D. Helmer, in First Steps of Animal Domestication,

New archaeozoological approaches J.-D. Vigne, J. Peters, D. Helmer Eds. (Oxbow

Books, Oxford, 2005) pp. 96-124.

A15. M. Rosenberg, M. R. Nesbitt, E. W. Redding, T. F. Strasser, Anatolica 21, 1 (1995).

A16. H. Hongo, R. H. Meadow, in Archaeozoology of the Near East IV, Proc. 4th int.

Symp. Archaeozoology of Southwestern Asia and adjacent areas M. Mashkour et al.

Eds. (Archaeological Research and Consultancy, Gröningen, 2000) pp. 121-140.

A17. M. Molist Montaña Ed. Tell Halula (Siria). Un yacimiento neolítico dell vallle

medio del Éufrates. Campañas de 1991 y 1992. (Ministerio de educacion y cultura,

Madrid, 1996) pp. 223.

A18. J.-D. Vigne et al. in Archaeozoology of the Near East IV, Proc. 4th int. Symp.

Archaeozoology of Southwestern Asia and adjacent areas M. Mashkour et al. Eds.

(Archaeological Research and Consultancy (Publicaties 32), Gröningen, 2000) pp.

52-75.

A19. J.-D. Vigne, I. Carrère, J. Guilaine, Bull. Corr. Héllenique suppl. 43, 239 (2003).

A20. D. Helmer, L. Gourichon, in Archaeozoology of the Near East VIII, Proc. 4th int.

Symp. Archaeozoology of Southwestern Asia and adjacent areas E. Vila, L.

Gourichon Eds. (Maison de l’Orient Méditerranéen, Lyon, in press).

A21. M. Saña Seguí, Arqueología de la domesticaión animal. La gestión de los recursos

animales en Tell Halula (Valle del Éufrates-Siria) del 8.800 al 7.000 B.P.

(Universitat Autònoma de Barcelona, Treballs d’Arqueologia del Pròxim Orient 1.

Barcelona, 1999) pp. 241.

A22. A. J. Legge, in The Origins and Spread of Agriculture and Pastoralism in Eurasia

D. R. Harris Ed. (Univ. College, London, 1996), pp. 238–262.

- 202 -
 Annex

A23. A. M. T. Moore, A. J. Legge, G. C. Hillman, Village on the Euphrates (Oxford

University Press, Oxford USA, 2000).

A24. J.-D. Vigne, H. Buitenhuis, Paléorient 25, 49-62 (1999).

A25. S. K. Koslowski, Nemrik 9 - Pre Pottery neolithic site in Iraq, (Inst. Archaeol.,

Warsaw, 1989-99) vol 1-5.

A26. D. Helmer, J.-D. Vigne, Anthropozoologica 42, 2, (in press).

A27. D. Zohary, E. Tchernov, L. Kolska Horwitz, J. Zool. Lond. 245, 129 (1998).

A28. J.-D. Vigne, in The Neolithic Demographic Transition and its Consequences J.-P.

Bocquet Appel, O. Bar-Yosef Eds. (Springer Verlag, New York, in press).

A29. J. Clutton-Brock, Domesticated animals. From early times (Heinemann - British

Mus. Nat. Hist., London, 1981).

A30. R. J. Braidwood, Iranica Antiqua 1, 3 (1961).

A31. D. Perkins Jr, in Report of the VIth International Congress of the Quaternary,

(1961), vol. 2 (Warsaw: Lodz: Panstwowe Wydawnictwo Naukowe, 1964) pp. 565-

572.

A32. D. Perkins Jr. Science 114, 1565 (1964)

A33. F. Hole, K. V. Flannery, J. A. Neely, Prehistory and Human Ecology of the Deh

Luran Plain. An Early Village Sequence from Khuzistan, Iran (Ann Abor:

University of Michigan, 1969).

A34. S. Bökönyi, Animal remains from Kermanshah Valley, Iran (Oxford, Oxford

University Press (1977).

A35. B. C. Hesse, Evidence for husbandry from the early neolithic site of Ganj Dareh in

Western Iran (Columbia University, Columbia, 1978).

- 203 -
 Annex

A36. H.-P. Uerpmann, Probleme der Neolithisierung des [Link] zum

Tübinger Atlas des Vorderen Orients (Wiesbaden: Dr. Ludwig Reichert Verlag,

1979).

A37. O. Bar-Yosef, R. H. Meadow, in Last Hunters, First Farmers: New Perspectives on

the Prehistoric Transition to Agriculture D. Price, A. B. Gebauer Eds (Santa Fe:

School of American Research Press, 1995) pp. 39-94.

A38. M. A. Zeder, Paléorient 25,11 (1999).

A39. M. A. Zeder, Journal of Archaeological Science 28, 61 (2001).

A40. M. A. Zeder, in The Fisrt Steps of Animal Domestication, J.-D. Vigne, J. Peters, D.

Helmer Eds (Oxford, Oxbow Books, 2005) pp. 125-146.

A41. M. A. Zeder, E. Emshviller, B. D. Smith, D. G. Bradley, Trends in Genetics 22, 139

(2006).

A42. M. A. Zeder, B. Hesse, Science 287, 2254 (2000).

A43. M. Mashkour, A. Mohaseb, K. Debue, in The Origins of State Organizations in

Prehistoric Highland Fars, Excavations atT all-e Bakun A. Alizadeh Ed. (Oriental

Institut Publications 128, Chicago. Illinois, 2006) pp. 101-105.

A44. S. Masuda, Iran 12, 222 (1974).

A45. M. Mashkour, J.-D. Vigne, unpublished data.

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Résumé
La chèvre (Capra hircus) est l’un des premiers ongulés domestiqués il y a plus de 10 000 ans dans le
croissant fertile. L’histoire de la domestication a été abordée par l’analyse comparée de la diversité
génétique des chèvres domestiques et de celle de son ancêtre sauvage (Capra aegagrus). Nous avons
tout d’abord mis au point une méthode standard permettant d’établir une nomenclature claire des
haplogroupes mitochondriaux, et aussi de définir de nouveaux haplogroupes lorsque cela s’avère
pertinent. Cette méthode a été utilisée pour analyser 2430 séquences d’ADN mitochondrial (fragment
HV1 de la région de contrôle), incluant 946 nouveaux échantillons issus de régions très peu étudiées
jusqu’ici (notamment le Croissant Fertile). Les haplogroupes mitochondriaux présentent une forte
diversité génétique qui est essentiellement distribuée entre haplogroupes au sein des régions
géographiques. Même avec un jeu de donnée aussi important que celui-ci, il est très difficile de
comprendre l’histoire de la domestication en se basant uniquement sur l’analyse des animaux
domestiques. L’étude conjointe de la diversité des chèvres et de leurs ancêtres sauvages (les aegagres)
ont apporté les informations permettant de reconstituer l’histoire de la domestication. Ces données ont
été acquises à partir de 487 aegagres issus de 43 localités recouvrant l’ensemble de l’aire de répartition
de l’espèce. Chez les 308 aegagres génétiquement proches des chèvres, nous avons trouvé la signature
d’une croissance démographique plus forte que chez les autres aegagres. Cela suggère un nouveau
scénario de domestication de la chèvre en deux étapes. La domestication sensu stricto aurait été
précédée d’une phase de gestion des troupeaux sauvages par l’homme (la pré-domestication). Ces
processus se sont déroulés sur une vaste zone comprenant l’Est de l’Anatolie, l’ensemble du Zagros, le
Plateau Iranien Central et le Nord Est de l’Iran, où les aegagres génétiquement proches des chèvres
sont toujours présents. L’analyse comparée de la diversité nucléaire et mitochondriale chez les chèvres
et les aegagres démontre qu’une grande partie de la diversité génétique sauvage a été capturée par les
domestiques. Il n’y a donc pas eu de goulot d’étranglement au moment de la domestication de la
chèvre. Ce scénario est très différent des modèles précédents qui mettaient en avant des processus à
échelle réduite, avec des centres de domestication très localisés et une forte réduction de diversité
génétique.

Abstract
The goat (Capra hircus) was one of the first domesticated ungulates in Fertile Crescent more than
10,000 years ago. For investigating the evolutionary history and domestication process of this species,
we studied its present genetic diversity and that of its wild progenitor, the bezoar (Capra aegagrus).
Initially, the study of 2430 individuals from all over the old world allowed us to characterize the
genetic diversity of domestic goats. This study included 946 new individuals from regions poorly
studied until now, mainly the Fertile Crescent. The analysis concerned the HVI segment of the control
region of the mtDNA. This large-scale study allowed to establish a clear nomenclature of the goat
maternal haplogroups and also to assess the pertinence of defining new haplogroups. We found a large
genetic diversity that was mainly distributed among goat haplogroups within geographical areas.
However, even with such a huge data set, it remains difficult to understand the domestication history
by the genetic analysis of domestic goats on its own. Therefore, to fully understand the domestication
process, we compared the polymorphism of 487 modern bezoars from 43 localities covering most of
their distribution areas to that of the 2430 goats. Based on mtDNA data, we found that 308 bezoars
were close relatives to the six goat mtDNA haplogroups. They showed a higher population growth rate
than other bezoars. This data supports a new two-step large-scale domestication scenario for goats.
After an early phase of sustainable management of wild herds by humans (pre-domestication phase),
the effective domestication took place over a large area. This area included Eastern Anatolia, the whole
Zagros, the Central Iranian Plateau and the North-Eastern of Iran where wilds close-to-domestics are
still present. The combined analysis of mtDNA and nuclear DNA polymorphisms for bezoars and
domestic goats, demonstrated that a large genetic diversity, corresponding to a large number of
mtDNA haplotypes, was captured at the initial step of the effective domestication. The first
domesticated goats were able to capture most of the genetic diversity of their wild ancestors and
clearly, the goats do not fit the bottleneck domestication paradigm. This scenario is very different from
previous models, which call for restricted domestication centres and population bottlenecks.

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