Workshop on Population and Speciation Genomics 2020 W.

Salzburger | Speciation

Speciation
by Prof. Walter Salzburger
Zoological Institute, University of Basel, Vesalgasse 1, 4051 Basel, Switzerland

Speciation is the evolutionary process by which novel species originate from earlier ones. This process ————————
DIVERSIFICATION
is, in principle, equivalent to the divergence of lineages — also called DIVERSIFICATION — at the level The accumulation of
(genetic) differences
of populations, but implies that new species have arisen from it. Speciation is responsible for the between two ore
evolution of the organismal diversity of life on Earth. more taxa through
time.

Species concepts SPECIMEN

An individual
There is no consensus in biology what precisely a species is. In practical terms, individuals are grouped organism used for
into species in order to categorize organisms and to give these categories names, which in turn scientific study or
display.
facilitates the identification of biological SPECIMENS. Species descriptions are usually done by
taxonomists, who classify species on the basis of shared morphological characters following taxonomy
GENE POOL
guidelines. Such diagnostic characters are then used to distinguish between members of different species Total number of
and to identify organisms, for example using field guides or identification keys. Species identification genes in an
interbreeding
can be cumbersome because of natural variation: Individuals within a species are variable and there is population at a given
usually no “ideal” or “typical” individual. Evolutionary biologists, on the other hand, interpret species time (and across all
individuals).
as independent evolutionary units. Accordingly, members of the same species share a GENE POOL and
fundamental evolutionary processes such as selection and DRIFT operate within a species.
(GENETIC) DRIFT
A number of formal definitions of the category species, so called species concepts, have been proposed Random changes in
allele frequencies in a
(see TABLE 1 for a selection). Not one of these species concepts provides a universally valid definition population.
of the category species. This situation is referred to as the ‘species problem’.
CLONES
Genetically identical
TABLE 1. Species concepts used to defi ne the category species (modifi ed after Coyne & Orr 2004; Zachos 2016). individuals derived
from the same
biological A species is a group of interbreeding natural populations that is reproductively isolated ancestor. Clones are
species concept from other such groups (Mayr 1963). the result of asexual
reproduction, which
is found in bacteria
cohesion A species is the most inclusive populations of individuals having the potential for and viruses, but also
in some metazoans
species concept phenotypic cohesion through intrinsic cohesion mechanisms (Templeton 1989). such as aphids,
cladocerans and
A species is a lineages (or a closely related sets of lineages), which occupies an adaptive rotifers.
ecological ————————
zone minimally different from that of any other lineage in range and which evolve
species concept
separately from all lineages outside its range (Van Valen 1976).

A species is a single lineage of ancestral-descendant lineages that evolve separately

evolutionary
from other such lineages and have their own evolutionary tendencies and historical fate
species concept
(Simpson 1961; Wiley 1978).

A species is the smallest monophyletic group of common ancestry (de Querioz &
phylogenetic
Donoghue 1988). A phylogenetic species is a basal cluster of organisms that is
species concepts
diagnosably distinct from other such clusters (Cracraft 1989)

The biological species concept (BSC) is the most widely accepted and applied species definition in biology.
According to the BSC, a species includes all those individuals that actually or potentially produce
fertile offspring; species are separated from other species on the basis of some sort of reproductive
isolation mechanism (see below). The BSC places the category species within the framework of
population genetics and explains why members of the same species resemble each other
morphologically (because they share a gene pool), but differ from members of other species. The BSC
works well in sexually reproducing multicellular organisms, but fails in asexual organisms (CLONES) or
in organisms with partially uniparental reproduction. Furthermore, the BSC deals badly with low

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 W. Salzburger | Speciation

levels of GENE FLOW between species or with RING SPECIES (FIGURE 1A). Other species concepts ————————
overcome some of these issues, yet have their own drawbacks. The cohesion species concept, for GENE FLOW
The movement or
example, which defines species on the basis of phenotypic cohesion through genetic and/or exchange of genes
demographic exchangeability, applies to asexual organisms and deals with low levels of gene flow; into or through a
population by
however, the term ‘phenotypic cohesion’ is only vaguely defined. The ecological species concept and interbreeding or by
the evolutionary species concept are similarly vague, rendering their usage impracticable. Phylogenetic migration and
subsequent
species concepts deal badly with PARAPHYLETIC SPECIES (FIGURE 1B) — a situation that appears to be interbreeding.
common in nature.
RING SPECIES
Two reproductively
(A) Ensatina eschscholtzii ssp. (B) isolated populations
are connected by a
geographic ring of
populations that
interbreed. No

image source: www.whyevolutionistrue.wordpress.com

picta morphological
platensis
character can be
used, except
arbitrarily, to divide
the ring into discrete
species. A division

image sources: wikimedia (2), pinterest

oregonensis
would be
croceater
Blue Tit Azure Tit Blue Tit
meaningless, as there
really is a continuum.
Parus caeruleus Parus cyanus Parus caeruleus
North Africa Eurasia Europe
PARAPHYLETIC
xanthoptica SPECIES
A species that
includes most but not
all descendant
populations of a
eschscholtzii klauberi common ancestor.
This situation can
occur when one
FIGURE 1. Problems with defining species. (A) Ring species containing various subspecies of the salamander Ensatina eschscholtzii population diversifies
in western USA (from: Stebbins 1994). (B) The blue tit (Parus caeruleus) is a paraphyletic species. The North African subspecies into a new species.
P. c. degener and P. c. ultramarinus are the sister group to the European Blue Tit (P. c. caeruleus) plus the Eurasian Azure Tit (P. ————————
cyanus) (from: Salzburger et al. 2002).

Reproductive isolation
The origin of species is a continuous process, during which an ancestral species gives rise to one or
more novel species. The process is completed with the establishment of reproductive isolation (FIGURE 2),
that is, the members of the new species do not, or cannot, interbreed anymore with members of the
ancestral species. Any mechanism that prevents gene flow between (newly emerging) species is called
isolating mechanism or isolating barrier.
Isolating barriers are grouped, according to when they operate during a reproductive cycle, into
premating, postmating prezygotic and postzygotic isolating barriers (BOX 1). Premating isolation mechanisms are

species A
ancestral
species

species B

reproductive
isolation no partial complete

time

FIGURE 2. The “speciation continuum”. A speciation event is completed once reproductive isolation is fully established. In this
example, two species (A and B) emerged out of the ancestral species; it is also called speciation, if the ancestral species continues to
exist and only one species emerged (in this case, either A or B would resemble the ancestral species).
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 W. Salzburger | Speciation

BOX 1: Isolating barriers (according to Coyne & Orr 2004).

Premating isolating barriers prevent the formation of a hybrid zygote by impeding gene fl ow before the transfer of
sperm or pollen:

Behavioral Mutual attraction between the sexes of different species is weak or absent, preventing
isolation them from initiating courtship or copulation.

Habitat isolation. The adaptation to different habitats in the same general area
prevents or limits gene exchange.
Ecological Temporal isolation. Gene fl ow between two taxa is impeded because of different
isolation breeding/fl owering times.
Pollinator isolation. Gene fl ow between angiosperm species is reduced by differential
interactions with pollinators.

Mechanical Copulation or pollination between two species is inhibited due to incompatibilities of

isolation reproductive structures.

Mating
The evolution of partial or complete self-fertilization or asexual reproduction prevents
system
gene flow with members of the ancestral population.
isolation

Postmating, prezygotic isolating barriers prevent the formation of hybrid zygotes after sperm or pollen transfer
but before fertilization:

Copulatory
The behavior of an individual during copulation is insufficient to allow normal
behavioral
fertilization.
isolation

Noncompetitive gametic isolation. Intrinsic problems with transfer, storage, or

fertilization of heterospecifi c gametes in single fertilizations between members of
Gametic different species.
isolation Competitive gametic isolation. Heterospecifi c gametes are not properly transferred,
stored, or used in fertilization when competing with conspecifi c gametes (“conspecifi c
sperm or pollen preference”).

Postzygotic isolating barriers reduce the viability or fertility of hybrid zygotes:

Ecological inviability. Hybrids develop normally but suffer lower viability because
they cannot fi nd an appropriate ecological niche.
extrinsic
Behavioral sterility. Hybrids have normal gametogenesis but are less fertile than
parental species because they cannot obtain mates.

Hybrid inviability. Hybrids suffer developmental diffi culties causing full or partial
lethality.
intrinsic Hybrid sterility. Hybrids suffer problems in the development of the reproductive
system or gametes or suffer neurological or physiological lesions that render them
incapable of successful courtship.

the most ‘inexpensive’, as there is no further investment into mating or reproduction. In cases where
hybrids feature a reduced fitness compared to pure-bread individuals, natural selection may act to
reinforce reproductive isolation due to the high costs of mating with a partner belonging to the
“wrong” species. The evolution of divergent mate preferences in response to selection against hybrids
is called reinforcement.

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The origin of species ————————

MUTATION
More than 150 years after the publication of Charles Darwin’s seminal book “On the Origin of Species”, Any change in the
nucleotide sequence
the questions of how and why isolating barriers and, consequently, new species emerge remain of an organism
challenging. Different modes and mechanisms of speciation have been identified. (compared to the
parental generation),
either in the form of
As initially proposed by Darwin, natural selection plays a key role in speciation. NATURAL a point mutation, a
SELECTION is generally recognized as central mechanism of evolutionary change within natural deletion/insertion, or
a chromosomal
populations; if selection is divergent — for example between habitats — two populations might be rearrangement.
driven apart and new species may form. The evolution of reproductive isolation between populations
by adaptation to different environments or ecological niches is called ecological speciation. Ecological ADAPTATION
speciation can occur in a variety of settings, including in allopatry, parapatry and sympatry (see below A feature of an
organism that evolved
for details). SEXUAL SELECTION can also lead to, or at least contribute to, speciation. Sexual selection is because it improves
one of the most potent forces mediating (premating) reproductive isolation; traits involved in mate the survival and
reproductive
choice, courtship and mating evolve faster than most other traits (see TABLE 2 for some fundamental performance of the
differences between natural and sexual selection). organism. Adaptation
may also refer to the
process that produces
such a feature.
TABLE 3. Fundamental differences between sexual and natural selection.
GENOME
selection based upon competitors The entire genetic
material of an
organism.
sexual selection individual fitness other members of the same sex

NATURAL
natural selection fitness of the genotype other individuals (within the same population) SELECTION
The process by which
the forms of
organisms in a
population that are
best adapted increase
A classical distinction relates to the different geographic conditions under which speciation may in frequency relative
occur (TABLE 3): A new species may arise in complete geographic — and, hence, genetic — isolation to the less well-
adapted forms over a
from its ancestor (allopatric speciation), it may form in a geographically contiguous setting (parapatric number of
speciation), or it may emerge within the geographic range of its ancestor (sympatric speciation). Historically, generations.
allopatric speciation (including its variants such as peripatric speciation) has been considered the default
SEXUAL SELECTION
mode by which new species evolve. In allopatric speciation, reproductive isolation emerges as The selection on
byproduct of independent evolution in geographically isolated populations. This may occur via drift, mating behavior,
the accumulation of different MUTATIONS, or ADAPTATION to different environments. The analysis of either through
competition among
GENOME wide data, on the other hand, suggests that the exchange of genetic material (gene flow) is members of one sex
rather common between diversifying populations. Parapatric speciation — either along environmental (usually males) for
access to members of
gradients (clines) or according to stepping stone models — may thus be way more common than previously the other sex or
through
thought. The frequency of occurrence of sympatric speciation is controversially discussed, not least choice by members
because — in many putative cases — alternative scenarios cannot be ruled out; however, mathematical of one sex (usually
females) for certain
models and computer simulations as well as empirical evidence (e.g., from cichlid fishes in small crater members of the other
lakes and palm trees on oceanic islands) suggest that it is common, too. The geographic modes of sex.
————————
speciation (allopatric, parapatric and sympatric) provide little information about the actual
mechanisms involved in the process.

TABLE 2. Geographic modes of speciation.

The origin of new species from geographically isolated populations; there is no gene
allopatric
exchange between the diverging populations (from Greek ‘allos’ = different, Latin ‘patria’ =
speciation
homeland).

The origin of new species from a peripherally isolated population (hence, a species case of
peripatric
allopatric speciation); there is no gene exchange between the diverging populations (from
speciation
Greek ‘peri’ = adjacent, Latin ‘patria’ = homeland).

The origin of new species from geographically adjacent populations; gene flow between
parapatric
diverging populations is neither zero nor the maximum possible (from Greek ‘para’ = alongside,
speciation
Latin ‘patria’ = homeland).

The origin of new species without geographic isolation; gene flow between diverging
sympatric
populations can be zero bus is usually neither zero nor the maximum possible(from Greek
speciation
‘syn’ = together, Latin ‘patria’ = homeland).

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New species may also originate via polyploidization or as a consequence of hybridization. ————————
POLYPLOIDS
POLYPLOIDS arise naturally, for example because of errors during meiosis (autopolyploidy) or after
Organisms that
HYBRIDIZATION events (allopoyploidy). The most common form of polyploidy in nature is tetraploidy. contain more than
Tetraploids are interfertile among themselves, but reproductively isolated from the parental species two homologous sets
of chromosomes such
(due to their different chromosomal arrangement). Hybrid speciation can occur when hybrids have a as triploids or
fitness advantage, for example under certain environmental conditions. Polyploid and hybrid tetraploids.
speciation are common in plants, but are also known from animals.
HYBRIDIZATION
Crossbreeding
between members of
two distinct taxa (e.g.,
populations, species,
genera)
————————

——————
References:
Coyne JA & HA Orr (2004) Speciation. Sinauer.
Nosil P (2012) Ecological speciation. Oxford.
Ridley M (2004) Evolution. Blackwell.
Zachos FE (2016) Species concepts in biology. Springer.
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