lecture xii genetics of speciation -...

Lecture XII Genetics of Speciation

Lecture WS Evolutionary Genetics Part I – Richard Merrill 1

Genetics of Speciation The evolution of new species – speciation – is the fundamental process that generates biodiversity … but it also is an inherently complex subject – Darwin’s ‘mystery of mysteries’. What are ‘species’? A good place to start is considering what a species is. This is more difficult than it sounds:- In some cases you can have dramatic amounts of convergence between different species, meaning they look the same. A famous example of this comes from these crater lake cichlids: the fish in the left column are more related to each other than to any of those in the right column (and vice versa), despite obvious morphological convergence (seen in each row). Conversely, closely related species may appear very similar – these are called cryptic species – these butterflies for example are the males (top) and females (bottom) of three distinct species, but they were only discovered by analysing genetic data. Finally, within some species there can be a large range of phenotypic variation - domesticated breeds of dogs are a good example of this. They can all interbreed, and they are all the same species.

Are species even real, or are they just an artefact of our human inclination towards categorising things? It is worth bearing in mind that speciation is (normally) a process: At what point have populations (perhaps referred ‘races’ or ‘subspecies’ etc. etc.) diverged enough to be considered different species? It has been suggested that a good analogy is the difference between ‘childhood’ and ‘adulthood’– we know there is a clear difference, but it’s hard to pinpoint the exact time when one becomes the other. Nevertheless, one of the most striking facts about biodiversity is that it is discontinuous; if we want to understand the evolutionary processes that have led to this, it is important to have a good (working) definition of a species. Many species concepts have been proposed – each with pros and cons – but as students of speciation we *normally* consider a (relaxed) Biological Species Concept, which was introduced by Ernst Mayr in 1942:

Species are groups of interbreeding populations, which are (normally) reproductively isolated from other such groups.

This is essentially a population genetics argument based on patterns of gene flow. It says that gene flow persists within species, but hybridisation and gene-flow are absent between species. But how does this hold up? Well actually not especially well … surprisingly hybridisation seems to be a natural part of species biology. Whilst hybridisation between (otherwise ‘good’) species is uncommon at an individual level, the number of species that occasionally hybridise with close relatives is high. For example, 75% of UK ducks, 6% of all European mammals and 25% of UK plants can produce viable offspring with closely related species (Mallet, 2008). Studies of Heliconius butterflies (and other species) suggests that this hybridisation can lead to substantial gene flow. Most would agree that H. melpomene and H. cydno are good species (e.g. there is strong assortative mating and differences in ecology); Simon Martin compared sympatric populations of H. melpomene and H. cydno (where hybridisation is known to occur) to a population of H. melpomene that occurs in the absence of H. cydno (and where there can be no hybridisation). Looking at phylogenetic trees for ‘sliding windows’ across the genome Simon was able to show that a high percentage follow the so-called ‘geography’ pattern (red ‘trees’), which clusters the two sympatric populations so that the allopatric population of H. melpomene is the out-group. (Though the ‘species’ tree = blue, which clusters the two melpomene populations, with cydno as the out-group, remains in the majority). This suggests that a high



proportion of the genomes of sympatric H. melpomene and H. cydno (perhaps up to 40%) are shared due to recent hybridisation and gene flow.

after Martin et al (2013) Genome Research

Despite all this the Biological Species Concept is useful – especially to those of us those interested in speciation – because it forces us to think about the evolution of reproductive barriers, i.e. those attributes that reduce gene flow across the species boundary.

Reproductive barriers: What keeps species separate?

Reproductive barriers are often classified into 2 categories – i) pre-zygotic ii) those post-zygotic. Prezygotic isolation occurs before the formation of the zygote (i.e. the cell formed by a fertilisation event between two gametes), and often before mating (strictly pre-mating rather than pre-zygotic, … when might barriers relating to sperm competition act?). These mechanisms stop individuals from divergent populations reproducing. These can be geographic or ecological barriers that prevent individuals meeting, or behavioural or mechanical barriers that mean that species don’t mate even if they do meet.

Postzygotic barriers occur after mating, so mating occurs but either the hybrids fail to develop, or develop with significant genetic problems due to incompatibilities or sterility. These sorts of incompatibilities can evolve by drift, as well as a result of by natural/sexual selection. (But how can alleles for inviability/sterility evolve under selection? More on this later.) Or the hybrids might develop relatively normally but may suffer a fitness deficit because they are intermediate between two parental phenotypes meaning they are not well suited to either parental environment (ecological post-zygotic isolation), or are not attractive to other individuals.

So those are the types of reproductive barriers that keep species apart. The rest of the lecture considers how reproductive barriers may evolve …

Geography. Speciation has traditionally been considered along geographical lines. That’s because geography can play a big role in speciation – indeed many researchers consider it the main cause of speciation, because it provides perhaps the simplest route to reproductive isolation. Allopatric speciation refers to situations where prolonged physical barriers impede gene flow between populations. If populations don’t meet each other, they cannot exchange alleles, that means over time, they can accumulate enough differences to become distinct species. This could be due to genetic drift alone – meaning that there is no need to invoke the hand of selection in creating new species. This might be most likely when a small part of a larger population becomes isolated, called peripatric speciation (because Ne is small => drift; think of a rare colonisation event of an island). However, differences resulting in reproductive isolation probably more often arise due to divergent natural selection, meeting the ecological requirements of different habitats (Ecological speciation – “the process by which barriers to gene flow evolve between populations as a result of ecologically based



divergent selection”, n.b. ecological speciation ≠ sympatric speciation). Selection could also drive speciation if populations fix distinct mutations that would nevertheless be advantageous in both of their environments, i.e. populations adapting to similar selection pressure by fixing different alleles, and this leads to reproductive isolation (Mutation-order speciation).

Alternatives to allopatric speciation include parapatric speciation, where there is divergence – perhaps caused by an environmental gradient - across a continuous population, and sympatric speciation where there is no extrinsic barrier at all. Recently, it has become less fashionable to talk about speciation in terms of allopatry, sympatry etc. This is perhaps due to the increased appreciation of speciation as a process, often involving the evolution of multiple reproductive barriers, which may occur under multiple geographical scenarios at different times. Even allopatric speciation is often thought to be completed under a mechanism that requires interbreeding – reinforcement (i.e. increase in pre-zygotic isolation in response to selection against unfit hybrids; aka the Wallace effect after Alfred Russel Wallace). It is now more common to talk about speciation with and without gene flow.

Why are there so few kinds of animals? Gene flow can aid speciation: Reinforcement, as well as many models of sympatric speciation depend on the production of hybrids with relatively low fitness; and of course, hybrid speciation relies on hybridisation. Nevertheless, in general, speciation with gene flow is considered more difficult than speciation without gene flow – Why?

What is it about hybridisation and gene flow that constraints the evolution of reproductive isolation? This question was robustly addressed in a famous paper by Joseph Felsenstein (1981): “Skeptism towards Santa Rosalia, or why are there so few kinds of animals”. He argued that if local adaptation is common, speciation would be ‘all but inevitable’ resulting in a “different species on every bush” – but because there are *so few* species there must be fundamental constraints. These constraints are genetic: Specifically, if gene flow persists, recombination will break down the genetic associations between alleles that characterise emerging species. Most models of speciation-with-gene-flow require a trait under divergent selection to become associated with a source of prezygotic isolation. More broadly, genome-wide linkage disequilibrium (LD) is a signature of speciation, reflecting the presence of barriers to gene exchange. So, in other words, when gene flow occurs between diverging populations, recombination opposes the build-up of LD between alleles (or will cause the breakdown pre-existing LD), preventing the formation of strong associations between isolating traits necessary for speciation (or disrupting associations previously formed in allopatry).

This antagonism between selection and recombination is a fundamental obstacle to the evolution of reproductive isolation, particularly when associations need to be generated between directly selected traits (e.g. those under divergent ecological selection) and those involved in prezygotic

Divergentselection Hybridizationandgeneflow



isolation (e.g. mating cues and/or preferences), which may be under indirect selection.

Felsenstein also recognised that reproductive isolation may be strengthened via two distinct processes, depending on whether reproductive isolation is increased by substituting the same or different alleles in the emerging daughter species:

- two-allele model = RI strengthened by substituting different alleles - one-allele model = RI strengthened by substituting same alleles

Importantly, speciation with gene flow is great facilitated under a one-allele process because recombination cannot break down the association between alleles under direct and indirect selection.

If speciation is easier via one-allele processes is there any empirical evidence that they occur in nature. Some of the best evidence comes from Daniel Ortiz-Barrientos’ studies of the fruit flies. Females from populations of D. pseudoobscura that co-occur with its sibling species, D. persimilis, exhibit greater reluctance to mate with D. persimilis males than females from populations that don’t co-occur with D. persimilis. They mapped the genetic basis of this behavioural difference among D. pseudoobscura populations to two chromosomal regions, including one on the fourth chromosome called Coy-2. To test if Coy-2 acts as a one-allele assortative mating locus, Daniel introgressed alleles from sypatric and allopatric D. pseudoobscura into D. persimilis and tested the females’ reluctance to mate with heterospecific males. Supporting a one-allele mechanism, D. persimilis females with the sympatric pseudoobscura allele were less willing to mate with heterospecific males than those with the allopatric pseudoobscura allele. Elsewhere, we might consider the spread of alleles causing individuals to sexually imprint on parental phenotypes, or alleles causing a reduction in migration rate, for example, to evolve through one allele mechanisms … though this might be harder to demonstrate experimentally (and the alleles involved may be ancestral – so not strictly involve the

Ecological trait

Matingtrait Ecological

trait

Matingtrait

Selection Selection

Two-allele model One-allele model

ParentalSpecies

DaughterSpecies

Selection

Two-allele model

Disassociation of alleles

interbreeding

DaughterSpecies

Reco

mbi

natio

n

Reco

mbi

natio

n

Selection

No Disassociation of alleles

interbreeding

DaughterSpecies

One-allele model



substitution of alleles that increase reproductive isolation).

What about the two-allele scenario? Are there mechanisms that might reduce the homogenising effects of gene-flow when different alleles are fixed in diverging populations? One of the most widely discussed is the idea of so-called ‘magic traits’. This simply refers to traits that contribute to prezygotic isolation, but which evolve under direct selection i.e. traits under divergent selection that also influence assortative mating. These traits clearly reduce the effects of recombination during the evolution of reproductive isolation: recombination cannot break down the associations between alleles when the trait involved are one and the same (and so influenced by the same alleles). These ‘magic’ or ‘multiple-effect’ traits were once thought to be very rare, and perhaps biologically unrealistic (leading Sergey Gavrilets (2004) to coin the dismissive term ‘magic traits’ in the first place); and typically include mating cues (such as colour or body size), which are also under divergent ecological selection. Now it is thought that they are probably common and have played a role in the speciation of a wide range of organisms (see Servedio et al. 2011). Nevertheless, it has proved difficult to experimentally demonstrate that magic traits exist in nature; as Maria Servedio (2011) states, ‘two criteria must be met for a trait to qualify as a magic trait. First, the magic trait, not a correlated trait (controlled by different genes), must be subject to divergent selection. Second, the magic trait, not a correlated trait, must generate non-random mating’. Using paper models (thereby controlling for other cues), Chris Jiggins (2001) was able to show that males prefer to court females with the same warning pattern as themselves. Again using paper models, I have demonstrated that these same patterns are under strong disruptive selection (Merrill et al. 2012). The amenability of Heliconius colour patterns to experimental manipulation has allowed us to the experimentally demonstration that colour pattern in these butterflies is a good example of a magic trait; but there are many other potential examples.

Another potentially mechanism is simply tight physical linkage: if loci are physically close on a chromosome recombination is less likely to break up associations between alleles. A potential example of this (which has been very recently published), concerns benthic (bottom dwelling) and limnetic (open surface dwelling) sticklebacks. These two ecotypes differ in body size and shape (which are under divergent ecological selection), and might be considered nascent species. Rachel Bay and colleagues (Current Biology, in press) mapped body morphology and female mate choice. They found that QTL influencing these two traits are co-localised in the genome – perhaps suggesting a physical association between the loci involved (though other interpretations are possible, which they discuss). Similarly, in Heliconius (sorry!) we have found that major loci affecting differences in colour pattern (the ‘magic trait’) and male preference also map to the same genomic region, suggesting very tight physical linkage. Physical linkage can be greatly enhanced by chromosomal structures – such as inversions – that locally reduce recombination (or other genomic modifiers). There is considerable evidence that structures such as these have played an important role in speciation – especially from Drosophila.

At one extreme of physical linkage, we might consider pleiotropy ( = ‘one allele affects two or more traits’). Pleiotropy has long been recognised as an ‘easy’ way to facilitate speciation with gene flow; in another famous paper, John Maynard-Smith (“Sympatric speciation”, 1966) recognised this, but dismissed it pretty quickly:



Pleiotropy has been suggested as a mechanism explaining co-segregation of preference and cue in a number of systems. One of the most convincing is probably in Hawaiian crickets, where QTL for variation in song and for variation in female preference for song map to the same genomic locations. Nevertheless, evidence of co-segregation of QTL is not good evidence of pleiotropy, especially because QTL will often include many genes – in most cases this still ‘seems very unlikely’. It is important to emphasise that pleiotropy is a property of an allele, not of a gene. Consequently, it is possible for one allelic substitution in a gene to influence two traits, while others influence only one of the traits, or neither. (And by extension magic/multiple-effect traits ≠ pleiotropy.)

It is worth noting that both one-allele and two-allele processes may act at the same time, at different loci. Similarly, different mechanisms might contribute to reduce the homogenising effects of gene flow thereby increasing the chance of speciation in the face of gene flow. Reproductive isolation is usually multi-genic and involves multiple components. Progresses towards cessation of gene exchange (i.e. speciation) likely involves the generation and maintenance of associations among multiple isolating traits. One way to think about this is to consider a ‘trait association chain’ (Smadja & Butlin 2011) – speciation becomes more likely as we i) reduce the number of links required to couple different components of reproductive isolation, and ii) strengthen those links that exist.

Finally, we consider the evolution of sterility and in-viability between populations. Sterility and/or inviabaility in the hybrid offspring of individuals between two populations will clearly reduce gene flow. However, it’s not obvious how sterility or inviability might be selected for – surely any alleles that result in sterility or inviability will be selected against. This problem is solved by the Dobzhansky-Muller 2-Locus model, (which leads to Dobzhansky-Muller Incompatibilities, or “DMI”s).

SYMPATRIC SPECIATION 643

1. Habitat selection

If in a heterogeneous environment mating takes place within the "niche"- perhaps because individuals tend to return to mate in the habitat in which they were raised (e.g., many bird species)-then the populations from two niches, whether genetically different or not, will be largely isolated. They could, therefore, evolve into separate species exactly as in the case of allopatric speciation. This should perhaps be regarded as a form of allopatric speciation in which isolation is behavioral rather than geographic.

But even if, as must usually be the case, the isolation between niches was only partial, it would favor the establishment of a stable polymorphism of the kind discussed in the last section; i.e., smaller selective coefficients would be required to maintain polymorphism.

Suppose, however, that initially no isolation exists between the two niches, the adults from both forming a single random-mating population. Then, once a stable polymorphism has been established, there will be selection in favor of habitat selection in both sexes, for the following reason. Individuals will tend to be adapted to the niche in which they were raised, because they did in fact survive in that niche. Their offspring will tend to resemble them. Therefore, if they have a genotype causing them to produce offspring in the same niche in which they were themselves raised, this will increase their fitness.

It follows that the establishment of a stable polymorphism may lead to isolation by habitat selection.

2. Pleiotropism The gene pair A, a adapting individuals to different niches may them-

selves cause assortative mating: i.e., A mating with A and aa with aa. This seems very unlikely.

3. Modifier Genes It is supposed that the original population, during the establishment of

the A, a polymorphism, had a genotype-say bb-such that mating was random. Mating isolation could arise by the replacement of b by B, so that for individuals of genotype B, there is assortative mating at the A locus. The situation is set out in Table 1, in which + indicates that mating occurs,

TABLE 1

Mating relations between genotypes resulting from the modifier gene B. + indicates mating; - indicates no mating.

genotype

A bb aabb AB aaB

A bb + + + + Genotype bb + + + +

A B + _ + aa B - + +

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Imagine you have an ancestral population with genotype AA and BB at two distinct loci. If these populations are isolated, a new allele a may emerge in one of the two populations, and eventually may become fixed due genetic drift or selection. If the two loci interact, a will only become fixed if it is compatible with BB. In the other population, a new allele b may emerge and become fixed at the other locus. Again, b will only spread in this population if it is compatible with AA genotypes. In a hybrid between these two populations a and b may co-occur for the first time. Since they have not evolved in the same population there is no guarantee that this combination of alleles will maintain the interaction between A and B. If it doesn’t these alleles are incompatible. And the hybrids may be inviable or suffer fitness deficits … allowing the evolution of sterility, inviability etc.

Literature

General references (mostly reviews):

Schluter, D. (2009) Evidence for ecological speciation and its alternative. Science 323: 737-741

Smadja, C.M. & Butlin, R. (2011) A framework for comparing processes of speciation in the presence of geneflow. Molecular Ecology

Servedio, M. et al (2011) Magic traits in speciation: ‘magic’ but not rare? TREE 26: 389-397 For those especially interested there many books on speciation: Coyne & Orr (2004) Speciation … and … Nosil (2012) Ecological Speciation … provide good overviews – with different empheses.

lecture xii genetics of speciation -...

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