Papers by Luciano Beheregaray
Island radiations can offer challenging systems for the implementation of conservation policies b... more Island radiations can offer challenging systems for the implementation of conservation policies because descendent populations may exhibit different levels of adaptive divergence, reproductive isolation, and phylogenetic distinctiveness. This seems particularly true for the endangered Galápagos giant tortoises (Geochelone nigra), which comprise a lineage that radiated rapidly and concomitantly with the evolution of the archipelago. We used mitochondrial DNA sequences and microsatellite markers to investigate the genetic structure, and to reconstruct genealogical relationships and the history of population colonization of giant tortoises from the Islands of Santa Cruz and Pinzón, including samples of a basal taxon from the Island of San Cristóbal. Populations displayed marked genetic divergence, contrasting demographic histories, and deep phylogeographic structure. The pattern of diversification among populations was consistent with geological and biogeographic history, and to some extent, with adaptive and morphological divergence. Results strongly indicate the presence of a minimum of four conservation units with long-standing evolutionary separation: two in Santa Cruz, one in Pinzón, and one in San Cristóbal. We propose that these findings be effectively integrated with other existing data by the appropriate environmental agencies to evaluate current conservation efforts and implement new strategies aimed at protecting the integrity and diversity of giant tortoise populations.
Animal Conservation, 2003
Giant tortoises once thrived throughout the Galápagos archipelago, but today three island populat... more Giant tortoises once thrived throughout the Galápagos archipelago, but today three island populations are extinct, only one individual survives from the island of Pinta, and several populations are critically endangered. We established the geographic origin of 59 captive tortoises housed at the Charles Darwin Research Station in the Galápagos Islands in an effort to find a mate for the sole survivor from Pinta (‘Lonesome George’) and to augment the number of breeders in other imperilled populations. By comparison with an extensive database of mtDNA control region (CR) haplotypes and nine microsatellites, we determined the geographic and evolutionary origin of the captive individuals. All individuals had CR haplotypes and multilocus microsatellite genotypes identical to or closely related to known haplotypes from natural populations. No obvious mate was found for Lonesome George, although we found several captive individuals carrying an evolutionarily close but geographically distinct mtDNA haplotype. Tortoises with mtDNA haplotypes closely related to another at-risk population (San Cristóbal) were also identified. These individuals could be considered as candidates for augmentation of natural populations or captive-breeding programmes and exemplify how molecular techniques can provide insights for the development of endangered species management plans.
Proceedings of The National Academy of Sciences, 2008
Giant tortoises, a prominent symbol of the Galá pagos archipelago, illustrate the influence of ge... more Giant tortoises, a prominent symbol of the Galá pagos archipelago, illustrate the influence of geological history and natural selection on the diversification of organisms. Because of heavy human exploitation, 4 of the 15 known species (Geochelone spp.) have disappeared. Charles Darwin himself detailed the intense harvesting of one species, G. elephantopus, which once was endemic to the island of Floreana. This species was believed to have been exterminated within 15 years of Darwin's historic visit to the Galá pagos in 1835. The application of modern DNA techniques to museum specimens combined with long-term study of a system creates new opportunities for identifying the living remnants of extinct taxa in the wild. Here, we use mitochondrial DNA and microsatellite data obtained from museum specimens to show that the population on Floreana was evolutionarily distinct from all other Galá pagos tortoise populations. It was demonstrated that some living individuals on the nearby island of Isabela are genetically distinct from the rest of the island's inhabitants. Surprisingly, we found that these ''non-native'' tortoises from Isabela are of recent Floreana ancestry and closely match the genetic data provided by the museum specimens. Thus, we show that the genetic line of G. elephantopus has not been completely extinguished and still exists in an intermixed population on Isabela. With enough individuals to commence a serious captive breeding program, this finding may help reestablish a species that was thought to have gone extinct more than a century ago and illustrates the power of long-term genetic analysis and the critical role of museum specimens in conservation biology.
Journal of Biology, 2007
DNA studies are revealing the extent of hidden, or cryptic, biodiversity. Two new studies challen... more DNA studies are revealing the extent of hidden, or cryptic, biodiversity. Two new studies challenge paradigms about cryptic biodiversity and highlight the importance of adding a historical and biogeographic dimension to biodiversity research.
Proceedings of The National Academy of Sciences, 2004
Isolated oceanic archipelagos have played a major role in the development of evolutionary theory ... more Isolated oceanic archipelagos have played a major role in the development of evolutionary theory by offering a unique setting for studying spatial and temporal patterns of biological diversification. However, the evolutionary events that cause associations between genetic variation and geography in archipelago radiations are largely unknown. This finding is especially true in the Galá pagos Islands, where molecular studies have revealed conflicting biogeographic patterns. Here, we elucidate the history of diversification of giant Galá pagos tortoises by using mtDNA sequences from 802 individuals representing all known extant populations. We test biogeographic predictions based on geological history and assess the roles of volcano emergence and island formation in driving evolutionary diversification. Patterns of colonization and lineage sorting appear highly consistent with the chronological formation of the archipelago. Populations from older islands are composed exclusively of endemic haplotypes that define divergent monophyletic clades. Younger populations, although currently differentiated, exhibit patterns of colonization, demographic variation and genetic interchange shaped by recent volcanism. Colonization probably occurs shortly after a volcano emerges through range expansion from older volcanoes. Volcanism can also create temporal shifts from historical to recurrent events, such as promoting gene flow by creating land bridges between isolated volcanoes. The association of spatial and temporal patterns of genetic variation with geophysical aspects of the environment can best be attributed to the limited dispersal and migration of tortoises following an oceanographic current. The endangered giant Galá pagos tortoises represent a rapid allopatric radiation and further exemplify evolutionary processes in one of the world's greatest natural laboratories of evolution.
Proceedings of The National Academy of Sciences, 2008
Giant tortoises, a prominent symbol of the Galá pagos archipelago, illustrate the influence of ge... more Giant tortoises, a prominent symbol of the Galá pagos archipelago, illustrate the influence of geological history and natural selection on the diversification of organisms. Because of heavy human exploitation, 4 of the 15 known species (Geochelone spp.) have disappeared. Charles Darwin himself detailed the intense harvesting of one species, G. elephantopus, which once was endemic to the island of Floreana. This species was believed to have been exterminated within 15 years of Darwin's historic visit to the Galá pagos in 1835. The application of modern DNA techniques to museum specimens combined with long-term study of a system creates new opportunities for identifying the living remnants of extinct taxa in the wild. Here, we use mitochondrial DNA and microsatellite data obtained from museum specimens to show that the population on Floreana was evolutionarily distinct from all other Galá pagos tortoise populations. It was demonstrated that some living individuals on the nearby island of Isabela are genetically distinct from the rest of the island's inhabitants. Surprisingly, we found that these ''non-native'' tortoises from Isabela are of recent Floreana ancestry and closely match the genetic data provided by the museum specimens. Thus, we show that the genetic line of G. elephantopus has not been completely extinguished and still exists in an intermixed population on Isabela. With enough individuals to commence a serious captive breeding program, this finding may help reestablish a species that was thought to have gone extinct more than a century ago and illustrates the power of long-term genetic analysis and the critical role of museum specimens in conservation biology.
Volcanic islands represent excellent models with which to study the effect of vicariance on colon... more Volcanic islands represent excellent models with which to study the effect of vicariance on colonization and dispersal, particularly when the evolution of genetic diversity mirrors the sequence of geological events that led to island formation. Phylogeographic inference, however, can be particularly challenging for recent dispersal events within islands, where the antagonistic effects of land bridge formation and vicariance can affect movements of organisms with limited dispersal ability. We investigated levels of genetic divergence and recovered signatures of dispersal events for 631 Galápagos giant tortoises across the volcanoes of Sierra Negra and Cerro Azul on the island of Isabela. These volcanoes are among the most recent formations in the Galápagos (,0.7 million years), and previous studies based on genetic and morphological data could not recover a consistent pattern of lineage sorting. We integrated nested clade analysis of mitochondrial DNA control region sequences, to infer historical patterns of colonization, and a novel Bayesian multilocus genotyping method for recovering evidence of recent migration across volcanoes using eleven microsatellite loci. These genetic studies illuminate taxonomic distinctions as well as provide guidance to possible repatriation programs aimed at countering the rapid population declines of these spectacular animals.
Conservation Genetics, 2003
Island radiations can offer challenging systemsfor the implementation of conservation policiesbec... more Island radiations can offer challenging systemsfor the implementation of conservation policiesbecause descendent populations may exhibitdifferent levels of adaptive divergence,reproductive isolation, and phylogeneticdistinctiveness. This seems particularly truefor the endangered Galápagos gianttortoises (Geochelone nigra), whichcomprise a lineage that radiated rapidly andconcomitantly with the evolution of thearchipelago. We used mitochondrial DNAsequences and microsatellite markers toinvestigate the genetic structure, and toreconstruct genealogical relationships and thehistory of population colonization of gianttortoises from the Islands of Santa Cruz andPinzón, including samples of a basal taxonfrom the Island of San Cristóbal.Populations displayed marked geneticdivergence, contrasting demographic histories,and deep phylogeographic structure. The patternof diversification among populations wasconsistent with geological and biogeographichistory, and to some extent, with adaptive andmorphological divergence. Results stronglyindicate the presence of a minimum of fourconservation units with long-standingevolutionary separation: two in Santa Cruz, onein Pinzón, and one in San Cristóbal. Wepropose that these findings be effectivelyintegrated with other existing data by theappropriate environmental agencies to evaluatecurrent conservation efforts and implement newstrategies aimed at protecting the integrityand diversity of giant tortoise populations.
Molecular Phylogenetics and Evolution, 2008
Proceedings of The Royal Society B: Biological Sciences, 2001
Marine Mammal Science, 2001
Sequence analysis of the mitochondrial DNA control region was used to clarify the taxonomic statu... more Sequence analysis of the mitochondrial DNA control region was used to clarify the taxonomic status of two coastal bottlenose dolphin populations from southeastern Australia currently classified as Tursiops truncatus. A 368-bp segment of the control region of 57 biopsy-sampled, photo-identified dolphins of Jervis Bay and Port Stephens was compared to published sequences of T. truncatus and T. aduncus from different oceanic regions. Sequence divergence between haplotypes from southeastern Australia and T. aduncus was much lower than that from T. truncatus. Analyses using two different methods of phylogenetic reconstruction unambiguously placed all haplotypes from southeastern Australia in a group composed exclusively of T. aduncus. The results strongly indicated that these two bottlenose dolphin populations belong to T. aduncus, extending the range of the species to subtropical waters of the Western South Pacific Ocean.
Marine and Freshwater Research, 2007
Oceanographic processes play a signiWcant role in shaping the genetic structure of marine populat... more Oceanographic processes play a signiWcant role in shaping the genetic structure of marine populations, but it is less clear whether they aVect genetic diVerentiation of highly mobile vertebrates. We used microsatellite markers and mtDNA control region sequences to investigate the spatial genetic structure of short-beaked common dolphins (Delphinus delphis) in southeastern Australia, a region characterised by complex oceanographic conditions associated with the East Australian Current (EAC). A total of 115 biopsy samples of dolphins were collected from six localities spanning approximately 1,000 km of the New South Wales (NSW) coastline. We found evidence for contrasting genetic diversity and Wne-scale genetic structure, characterised by three genetically diVerentiated populations with varying levels of admixture. Spatial genetic structure was not explained by a model of isolation by distance, instead it coincides with main patterns of oceanographic variation along the EAC. We propose that common dolphins along the EAC may be adapted to three water masses recently characterised in this region.
Kinship has been shown to be an important correlate of group membership and associations among ma... more Kinship has been shown to be an important correlate of group membership and associations among many female mammals. In this study, we investigate association patterns in female Indo-Pacific bottlenose dolphins (Tursiops aduncus) inhabiting an embayment in southeastern Australia. We combine the behavioral data with microsatellite DNA and mitochondrial DNA data to test the hypotheses that genetic relatedness and maternal kinship correlate with associations and social clusters. Mean association between females was not significantly different from a random mean, but the standard deviation was significantly higher than a random standard deviation, indicating the presence of nonrandom associates in the dataset. A neighbor-joining tree, based on the distance of associations between females, identified four main social clusters in the area. Mean genetic relatedness between pairs of frequent female associates was significantly higher than that between pairs of infrequent associates. There was also a significant correlation between mtDNA haplotype sharing and the degree of female association. However, the mean genetic relatedness of female pairs within and between social clusters and the proportion of female pairs with the same and different mtDNA haplotypes within and between clusters were not significantly different. This study demonstrates that kinship correlates with associations among female bottlenose dolphins, but that kinship relations are not necessarily a prerequisite for membership in social clusters. We hypothesize that different forces acting on female bottlenose dolphin sociality appear to promote the formation of flexible groups which include both kin and nonkin.
Molecular Ecology, 2004
In most mammals males usually disperse before breeding, while females remain in their natal group... more In most mammals males usually disperse before breeding, while females remain in their natal group or area. However, in odontocete cetaceans behavioural and/or genetic evidence from populations of four species indicate that both males and females remain in their natal group or site. For coastal resident bottlenose dolphins field data suggest that both sexes are philopatric to their natal site. Assignment tests and analyses of relatedness based on microsatellite markers were used to investigate this hypothesis in resident bottlenose dolphins, Tursiops aduncus, from two small coastal populations of southeastern Australia. Mean corrected assignment and mean relatedness were higher for resident females than for resident males. Only 8% of resident females had a lower probability than average of being born locally compared to 33% of resident males. Our genetic data contradict the hypothesis of bisexual philopatry to natal site and suggest that these bottlenose dolphins are not unusual amongst mammals, with females being the more philopatric and males the more dispersing sex.
Behavioral Ecology and Sociobiology, 2006
Kinship has been shown to be an important correlate of group membership and associations among ma... more Kinship has been shown to be an important correlate of group membership and associations among many female mammals. In this study, we investigate association patterns in female Indo-Pacific bottlenose dolphins (Tursiops aduncus) inhabiting an embayment in southeastern Australia. We combine the behavioral data with microsatellite DNA and mitochondrial DNA data to test the hypotheses that genetic relatedness and maternal kinship correlate with associations and social clusters. Mean association between females was not significantly different from a random mean, but the standard deviation was significantly higher than a random standard deviation, indicating the presence of nonrandom associates in the dataset. A neighbor-joining tree, based on the distance of associations between females, identified four main social clusters in the area. Mean genetic relatedness between pairs of frequent female associates was significantly higher than that between pairs of infrequent associates. There was also a significant correlation between mtDNA haplotype sharing and the degree of female association. However, the mean genetic relatedness of female pairs within and between social clusters and the proportion of female pairs with the same and different mtDNA haplotypes within and between clusters were not significantly different. This study demonstrates that kinship correlates with associations among female bottlenose dolphins, but that kinship relations are not necessarily a prerequisite for membership in social clusters. We hypothesize that different forces acting on female bottlenose dolphin sociality appear to promote the formation of flexible groups which include both kin and nonkin.
Molecular Ecology Notes, 2006
An inefficient aspect of marker identification from microsatellite-enriched libraries is the prop... more An inefficient aspect of marker identification from microsatellite-enriched libraries is the proportion of clones with identical sequences. This can substantially increase the number of clones that need to be sequenced in order to identify a sufficient number of microsatellite loci. We propose the use of single-stranded conformation polymorphism (SSCP) analysis to identify unique clones prior to sequencing. We used this approach prior to sequencing from microsatellite-enriched libraries for three marine invertebrate species and were able to obtain a given number of unique clone sequences for only 28% of the sequencing effort that would have been required without SSCP screening.
Ecology, 2007
Understanding the scale of marine population connectivity is critical for the conservation and su... more Understanding the scale of marine population connectivity is critical for the conservation and sustainable management of marine resources. For many marine species adults are benthic and relatively immobile, so patterns of larval dispersal and recruitment provide the key to understanding marine population connectivity. Contrary to previous expectations, recent studies have often detected unexpectedly low dispersal and fine-scale population structure in the sea, leading to a paradigm shift in how marine systems are viewed. Nonetheless, the link between fine-scale marine population structure and the underlying physical and biological processes has not been made. Here we show that patterns of genetic structure and population connectivity in the broadcast-spawning and long-distance dispersing sea urchin Centrostephanus rodgersii are influenced by physical oceanographic and geographic variables. Despite weak genetic differentiation and no isolation-by-distance over thousands of kilometers among samples from eastern Australia and northern New Zealand, fine-scale genetic structure was associated with sea surface temperature (SST) variability and geography along the southeastern Australian coast. The zone of high SST variability is characterized by periodic shedding of eddies from the East Australian Current, and we suggest that ocean current circulation may, through its influence on larval transport and recruitment, interact with the genetic consequences of large variance in individual reproductive success to generate patterns of fine-scale patchy genetic structure. If proven consistent across species, our findings suggest that the optimal scale for fisheries management and reserve design should vary among localities in relation to regional oceanographic variability and coastal geography.
Proceedings of The Royal Society B: Biological Sciences, 2002
Marine Ecology-progress Series, 2008
Recent studies of connectivity in marine populations have suggested that larval retention and loc... more Recent studies of connectivity in marine populations have suggested that larval retention and local recruitment are more common than previously considered. Here we used genetic data to investigate the scale of connectivity and patterns of recruitment in the abalone Haliotis coccoradiata, a broadcast spawner with a short larval stage. Although we detected weak but significant genetic differentiation (F ST ) between populations over a scale of approximately 1000 km, the pattern did not fit an isolation-by-distance (IBD) model, suggesting relatively long dispersal distances. However, individual-based multilocus spatial autocorrelation identified fine-scale genetic structure within a range of 20 km, suggesting short distance dispersal and local recruitment. Simple computer simulations in which all dispersal was restricted to within this scale (mean 10 km) suggested that a significant IBD result would most likely be generated under such a dispersal scenario. The lack of a significant IBD suggests infrequent long-distance dispersal is also likely and this is further supported by oceanographic particle dispersal modelling, which shows that larvae could be transported over large distances by ocean currents. Our results suggest that recruitment occurs primarily over a small spatial scale in a species that also has the ability to disperse over considerably greater distances.
Uploads
Papers by Luciano Beheregaray