speciation

After reading yesterday's penguin post, one of my readers thought I'd given up the ghost on the molecular clock.

But notice the bottom line of that message: those ancient penguins didn't tell us any thing new about the rate of mitochondrial changes over 10s of thousands of years. The rate, over at that time period, is pretty much what you would expect from comparing humans, or comparing Neandertals. Considering that the generation-to-generation rate of mutations of the mitochondrial DNA is maybe an order of magnitude higher, I'd say that consistency is pretty impressive.

Much more important, when it comes to comparing humans and chimps, we've come billions of base pairs beyond the mitochondrial DNA alone. We have drafts of the complete the numbers of humans and chimpanzees, macaques, and working drafts for gorillas, orangutans, and a handful of other primates. We have a better ability than ever to reconstruct the phylogenetic relationships of those species, the times that they diverged from each other, and even something about the number of individuals and structure of their ancient populations.

For the past five years, almost every study including more than a single gene has agreed on one central fact: humans and chimpanzees last exchanged genes less than 6 million years ago. Most of them place the date much younger -- an average of less than four and a half-million years ago.

Still, these kinds of comparisons can be quite complicated, and many -- maybe most -- of my paleoanthropology colleagues would prefer to remain ignorant of the details.

I can kind of sympathize. If somebody is willing to say it could be 6 million years, well, that doesn't sound so different from seven. And Sahelanthropus is only seven. What's the problem anyway?

I've got to say, though, that attitude is a fundamental lack of seriousness about the data. It's like if I said about Lucy, "Hey it's just a pelvis, right, what's the big deal?"

Well, it's the evidence, that's what. A. afarensis is a large and substantial sample with dozens of shared homologous features with humans and other hominins. If the genetics told us that humans and chimpanzees diverged less than 2 million years ago that would be a substantial conflict. Either that estimate would be wrong, or much of what we thought we knew about the pattern of hominin evolution would be.

We are in fact at that point in genetics. If the human-chimpanzee divergence really were much older than 5 million years ago, then much of what we think we know about population genetics of primates must be wrong.

I understand that many of my readers might welcome that suggestion. I, on the other hand, am having a hard time figuring out just how I'm supposed to make the divergence date much older than the current best estimates. In the 1990's, it was fashionable to just say that the clock was wrong, because our estimates of mutation rate were wrong, and leave it at that. People even did silly things like provide "confidence intervals" based on different assumptions about the human-orangutan divergence. If it was 12 million years ago, you'd get one (low) answer; if it were 16 million years ago, you'd get another (high) answer. Report the low and high ends, there's your "confidence" interval. Human-chimpanzee divergence: 4 to 6 million years.

It was a joke, but that's where things stood.

Nowadays, we know an awful lot more about the relations of these populations. I'm going to point everybody to a recent review paper -- it was released the same week as Ardipithecus was -- by Adam Siepel, in Genome Research. It's a very good review of the recent literature on the human-chimpanzee divergence, and by implication the human-gorilla and other primate divergences. It is not about building a phylogenetic tree -- it's about how we use sequence data from many genes to put together a phylogenomic tree, one that involves the divergences of populations and also their inbreeding and selection characteristics.

The time we estimate for a population divergence depends on the size of the ancestral population, as well as the pattern of selection within it. These factors also affect the sorting of gene variants of the ancestors into the descendant populations. As Siepel points out, these effects have led to two different methods of examining the demography and divergence times of ancient species:

Two simple, but ingenious, approaches were proposed early on, both of which exploited the fact that, with sparse sampling across the genome, the loci under study were likely to be unlinked, and their genealogies could be assumed to be statistically independent. The first method, by Takahata (1986), derived information about ancestral population sizes from the variance in the estimated divergence times for pairs of orthologous sequences. The second, by Wu (1991) (see also Hudson 1983a; Nei 1987), made use of the variance in tree topologies estimated from three or more orthologous sequences. Takahata's method essentially estimated [population divergence time] and [effective size] from the variance in estimates of [genetic divergence time] at multiple loci (in the notation above), while Wu's method estimated [effective size] from the relative frequency of topological inconsistency in reconstructed gene trees.

Those topological inconsistencies began to show up during the 80's and 90's, when people would publish sequences that favored human-gorilla or chimpanzee-gorilla clades. These were genes in which humans really were more closely related to gorillas, because the human-chimpanzee (chuman) ancestral population was large enough to retain two divergent alleles for the two million or so years that chumans existed.

Siepel goes on to review the literature using variants of these two approaches during the last seven or eight years. The Nature chimp-human hybridization paper by Patterson and colleagues (2006, which I reviewed here) forms a central part in the discussion, as people have reacted to that paper and the major issue it raised.

Reading the review, one cannot help but notice the low age estimates that keep coming up again and again. Most of them are under 4.5 million years. Patterson and colleagues had one of the highest recent estimates, putting the speciation at less than 5.4 million years. That's because they assume a smaller effective size in the ancestral lineages -- pushing the date higher. The more that demography fiddles with the assortment of ancestral genes before a population divergence, the younger the resulting estimate of divergence date will be.

To make the date older, you need to assume there was no demography -- an extreme chuman bottleneck. But that would be inconsistent with the evidence of incomplete lineage sorting -- those gorilla genes that we share. And it would take some magical rate discontinuities among genetic loci to get them the amount of interlocus variability that they have.

The review mentions some recent work suggesting that background selection may have reduced the site diversity in the ancestral species -- work to explain why the human X chromosome is even more similar to chimpanzees than the autosomes. Taken to an extreme, background selection or massive hitchhiking could raise the divergence estimate a bit, but it doesn't overcome the issue of incomplete lineage sorting, either.

You could push the human-orangutan divergence higher, or the human-macaque divergence, both of which help to calibrate the mutation rate. But that's not going to make 4 million years into 8 million, not unless orangutans diverged from us in the Oligocene.

You could propose a massive slowdown in mutations in the chuman lineage. But why? How? Like I said earlier, you'd have to change something pretty fundamental about our understanding of primate genetics.

No, it's very hard to see how these dates are going to get much older. What I'm saying is that you can't just wave them away; these are serious estimates and I don't see any simple way to get a better one.

Now, the question is, do the geneticists insufficiently appreciate the hominins? Do they just not care about the havoc this wreaks in paleoanthropology-land?

In fact, Siepel addresses this issue. The review mentions that Patterson and colleagues (2006) offered their hybridization idea in part to explain the early "hominin", Sahelanthropus. With the revelation of Ardipithecus' postcranial anatomy, I don't think we need to resort to chuman hybrids.

I think it's more parsimonious to imagine a widespread population of chumans, a large-bodied, basically Ardipithecus-like primate, structured into regional populations in much the way that today's chimpanzees and gorillas are. This population was numerous and stable, and it gave rise over time to many more arboreally adapted branches -- first the gorillas and later the chimpanzees. The remainders, as it were, became the hominins.

There are various hangups with this scenario that make me hesitate. I do take Orrorin seriously, for example -- it is hard to accommodate a 6-million-year old hominin under the large-population recent-divergence hypothesis.

And on the genetic side, the substitution rate in the nuclear genome is affected by positive selection, background selection, duplications and unequal crossing over. It's quite possible that some odd demographic scenario might reduce the genetic divergence date yet further, or increase it to some extent.

What's encouraging is that today's dense genetic data and fast modeling give us the chance to test these scenarios. We can model selection and demography directly and comparing results to observed genetic patterns.

OK, it's bedtime. More on this later...

References:

Siepel A. 2009. Phylogenomics of primates and their ancestral populations. Genome Res 19:1929-1941. doi:10.1101/gr.084228.108

You know I like the lizard analogies for human evolution -- I wrote about limb length and predation last time around -- and now we have another paper from Jonathan Losos' group looking at ecological differentiation and sexual dimorphism:

Sexual dimorphism is widespread and substantial throughout the animal world (1, 2). It is surprising, then, that such a pervasive source of biological diversity has not been integrated into studies of adaptive radiation, despite extensive and growing attention to both phenomena (1, 3, 4, 5, 6, 7). Rather, most studies of adaptive radiation either group individuals without regard to sex or focus solely on one sex. Here we show that sexual differences contribute substantially to the ecomorphological diversity produced by the adaptive radiations of West Indian Anolis lizards: within anole species, males and females occupy mostly non-overlapping parts of morphological space; the overall extent of sexual variation is large relative to interspecific variation; and the degree of variation depends on ecological type. Thus, when sexual dimorphism in ecologically relevant traits is substantial, ignoring its contribution may significantly underestimate the adaptive component of evolutionary radiation. Conversely, if sexual dimorphism and interspecific divergence are alternative means of ecological diversification, then the degree of sexual dimorphism may be negatively related to the extent of adaptive radiation.

These anoles have evolved into four different ecomorphs repeatedly on different islands of the Greater Antilles, and the sexes differentiate not only in their morphology but also their habitat use and diet.

Primates are generally group foragers, and because they forage together, males and females eat the same foods a lot of the time. The major components of sexual dimorphism across primates have mostly been considered in relation to body size and canine dimorphism, both of which have a strong social import, but less obvious ecological import. That is an apparent contrast to the anoles, whose dimorphism allows males and females to specialize to slightly different niches.

But even though body size and canine size are the main elements of dimorphism that can be compared across all primates, both these features and others may take on ecological importance within primate species. For one thing, sexual dimorphism leads to ecological differentiation even within foraging groups -- not necessarily because different sized individuals can exploit different foods, but because large individuals have preferential access. This has clear dietary and behavioral import -- for example, hunting is a social activity in chimpanzees; males hunt and females don't, and if a female did hunt (with males around), the males would probably take away the kill. That's not entirely because males are larger, but sexual dimorphism helps to determine the social ecology.

What about hominids? In the Plio-Pleistocene, there were at least three sympatric species of hominids in East Africa (and possibly more) and at least two in South Africa (and possibly more). These species were differentiated by body size, relative brain size, and masticatory adaptations. In other words, they occupied different ecologies involving different foods, and natural selection reinforced their ecological differences (even if the average diet involved much overlap, as I reviewed earlier).

The robust species in East Africa (A. boisei) appears to have had substantial body size dimorphism. The habiline species (H. habilis) was either substantially dimorphic, or was actually composed of two species. The large-bodied Homo may have had reduced dimorphism comparable to that in recent humans. Yet, many people have suggested that this least dimorphic species should have been the one where males and females had the greatest ecological differentiation. This is based on analogy with recent hunter-gatherers, assuming that the introduction of meat in substantial quantities requires a sexual division of labor.

Male and female lions have substantial body size dimorphism, and they are ecologically differentiated by prey size. Just thinking out loud...

References:

Butler MA, Sawyer SA, Losos JB. 2007. Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 447:202-205. doi:10.1038/nature05774

The story of colonizing species encompasses a wide range of "colonizing ability". From attempts at deliberate introductions, we know that some species just don't have a great potential to colonizing new territory; others succeed for a while and then explode.

We don't know the number of failed accidental introductions, but we do know a lot about one extreme -- the accidental introductions of alien species that become invasive problems. Such species have such a high colonizing potential (at least in certain contexts) that their populations explode beyond the numbers in their native ranges.

Brown (1957), discussing the colonizing ability of populations at the center of population ranges, brings in a number of examples of such invasive species, whose spread is often apparent within the span of decades or even years. One of these is the invasion and spread of the fire ant into North America.

Fire ants were inadvertently imported to the U.S. from South America sometime around 1918. Wilson (1953) gave an account of the early population history of these ants. It was clear in these early years that there were two forms of the ants, a dark-colored form and a red form. Of these, the red form was the more invasive, but it appeared that the real invasive character of the population might be attibutable to hybridization between the two. Brown (1957:259) quoted Wilson (1953):

For about ten years [the Mobile population] remained both genetically homogeneous, corresponding to the dark southern race richteri Forel of the South American parental population, and relatively unsuccessful in its new surroundings. In the period following 1930 a smaller reddish form rose to abundance, interbred extensively with the original dark form, and apparently precipitated the species' explosive increase to pest proportions. By 1949 the reddish form had largely replaced the dark form, which had become limited principally to the southern strip of the main population and part of its eastern and western periphery and to two outlying, isolated populations in Mississippi.

To this, Brown (1957:260) added:

The dark-phase colonies are now limited to certain separated peripheral areas of the range and a few minor enclaves within the main area of infestation, and even where they occur, they are often in the minority. All degrees of intergration [sic] link dark and red phases. As the red forms press outward, the dark forms apparently suffer both genetic swamping and competition-aggression, and consequently tend to extinction in most habitats. In spite of these forces at work against it, the dark form persists, genetically embedded, so to speak, in the dense and expanding matrix of red populations. This case is very instructive in showing how, regardless of its origin in this particular case, a genetic change actually spreads from a central point of introduction and tends in this way to cause a central-peripheral differential.

For Brown, the entire case of fire ant invasion is an evidence for central species having a greater colonizing potential than peripheral ones, because the tropical Solenopsis species were displacing congeneric S. geminata and S. xyloni, which had been common throughout the Caribbean and Gulf of Mexico coastal areas. The entire New World, from the point of view of Solenopsis is a zone with a tropical center and subtropical and temperate peripheries. In this case, Brown proposed that the displacement of fire ants from a central area (southern Brazil or Argentina) to the northern periphery had enabled the invasive character of the spread, although with probable adaptive changes in the new colonizing population.

The other element of this argument is that populations face more competition from similar competitor species and more natural disease and predation in the central parts of their ranges. Where a species can exist at higher densities, it can support more parasites, pathogens, and predators. For fire ants, these predators and parasites include a number of species that have been deliberately introduced as part of efforts to control their spread in the U.S.

Fire ant dispersal in southern U.S. from ca. 1939 to 1995. Figure from Brown 1957 p. 260. Brown took the plot from Wilson (1951).

I looked at that figure and gasped -- imagine living in one of the outlying counties in 1949 and knowing that pattern of spread.

Of course, from there the dispersal simply exploded. A good review of the history of fire ant spread was given by Anne-Marie Callcott and Homer Collins (1996). Their maps of infested counties over time say it all:

Fire ant dispersal in southern U.S. from ca. 1939 to 1995. Figures from Callcott and Collins 1996, pp. 244-246, recompiled for web format.

By the 1970's it was understood that the two forms of invasive fire ants had been two species (the dark form, Solenopsis richteri and the red Solenopsis invicta). The differentiation between the two at the colonizing edges of the fire ant wave is a genuine hybrid zone. Shoemaker and colleagues (1996) sampled the genetics of ants in this hybrid zone, finding that genetic markers and morphological characters introgressed at different rates, and that there appeared to be selection against hybrids in contact with one or the other parental type.

Later, Ross and Shoemaker (2005) studied the genetics of these South American species (S. richteri and S. invicta) in their native ranges. They found that the species were fully reproductively isolated at study sites where both were found. Additionally, the extent of genetic differentiation between different populations of each, and the presence of a third closely related species (S. quinquecuspis) led them to suggest that the group "is actively radiating species". This would be a confirmation of Brown's (1957) argument for the high speciation potential of the central populations in the range of this genus. It remains to be seen whether these central populations have actively generated new colonizing species to displace more peripheral populations by natural movement.

In the case of fire ants, the rapid colonization of the North American invaders has been aided by some unique social changes, described by Kenneth Ross and colleagues (1996). Probably most people think of ant colonies as having a single queen and many workers and soldier ants. But some kinds of ants form colonies with multiple queens. Imported fire ants have both single-queen and multiple-queen colonies, but the size and proportion of multiple-queen colonies has greatly increased relative to their South American range. This reduces intercolony competition and facilitates their spread compared to native species.

Later work has shown that S. invicta has a genetic switch that determines whether queens will form their own colonies or whether they will remain in their natal colony or attempt to join a new one. The system is described by Tsutsui and Suarez (2003):

Queens from the two social forms typically possess different genotypes at the general protein-9 (Gp-9) allozyme locus (Ross 1997; Ross & Keller 1998; Krieger & Ross 2002 ). Monogyne colonies contain queens that are BB at Gp-9 and produce new BB queens that disperse and found colonies independently (Shoemaker & Ross 1996). Conversely, the queens in polygyne colonies are almost exclusively Bb and can produce BB, Bb, and bb queens. New Bb queens either join their natal colony or attempt to join other polygyne colonies (DeHeer et al. 1999). Any BB queens that attempt to join polygyne colonies or reproduce within them are killed by the Bb workers present in polygyne colonies (Ross & Keller 1998). Studies of queen dispersal have shown that newly produced polygyne queens with the BB genotype, who are doomed to execution if they remain in their natal colony or attempt to join other colonies, may attempt to found colonies independently, but with limited success (DeHeer et al. 1999). The bb genotype appears to be lethal in workers, and fertile bb queens are extremely rare (Ross 1997; but see DeHeer et al. 1999; Goodisman et al. 2000. Interestingly, polygyne colonies in the native range can possess reproductive queens that are either BB or Bb (Keller & Ross 1999). This difference between native and introduced populations could indicate the presence of other undiscovered genes or alleles that affect queen number or could be the result of a genetic bottleneck on variation at the loci involved in this process (Keller & Ross 1999; Krieger & Ross 2002).

This is an interesting case with several elements. A simple genetic strategy is held polymorphic because the homozygotes for the multiple-queen strategy are completely nonviable. In the new founder populations, this allele might be lost completely. Also, possible modifier loci may lose alleles that restrain the formation of supercolonies in their native range.

Still, when it comes to social changes of invasive ants, nothing compares to the case of the Argentine ant (Linepithema humile). Like fire ants, the Argentine ant invaded the American South, becoming common early in the 1900's. They have also invaded California and the Southwest as well as five of the other six continents (sparing Antarctica...). In Argentine ants, the genetic uniformity of new colonizing populations is so great that the ants form supercolonies stretching across large areas. Here's a passage from a review paper by Neil Tsutsui and Andrew Suarez (2003):

Throughout their introduced range Argentine ants are highly unicolonial ( Newell & Barber 1913; Markin 1970; Keller & Passera 1989; Way et al. 1997; Suarez et al. 1999; Tsutsui et al. 2000; Giraud et al. 2002) and can attain remarkably high densities. For example, in an early attempt to eradicate Argentine ants from a 19-acre ( 7.7-ha) orange grove in Louisiana, Horton (1918 )reported trapping an astounding 1.3 million queens in artificial nest boxes over the course of 1 year. Including workers and brood, the total volume of Argentine ants collected was over 1000 gallons (Horton 1918). Although a single "supercolony" occupies virtually the entire Californian range ( Tsutsui et al. 2000), close examination has revealed several smaller "secondary" colonies (Holway et al. 1998; Tsutsui & Case 2001). The secondary colonies are spatially restricted, aggressive toward one another and toward the large supercolony, genetically distinct from one another and the large supercolony, and may be the result of separate introductions or genetic drift (Suarez et al. 1999; Tsutsui et al. 2001).

Yuck! Looking at the 20 inches of snow lining my yard is a whole lot easier when I consider how few invasive ant species have come from Siberia.

The invading Argentine ants have an even more substantial reduction in genetic diversity than fire ants, with heterozygosity being reduced to a third of its value in the native range of the ants. Not only founder effects, but also unique patterns of social behavior and selection maintain this low diversity. There is selection against genetically different colonies, who are outcompeted by supercolonies of genetically similar lineages. Also, a phenomenon called "queen execution" tends to increase the relatedness of individuals within colonies by eliminating a proportion of reproductives.

Tsutsui and Suarez (2003) present a good argument for understanding the genetics of this transformation to highly invasive phenotypes:

Finally, there are dozens of introduced ant species about which virtually nothing is known (McGlynn 1999). Many of these species may have the potential to become invasive, and prevention may be possible only if we are aware of their dispersal capabilities (both natural and human-mediated) and the factors that could facilitate their successful establishment and spread.

Invasive fire ants have recently reached California and are busily displacing the Argentine ants there. After reading through a number of articles, the final message of many of them has been that invasive species will ultimately be controlled only by the arrival of new invasive competitors.

Yippee.

References:

Brown WL, Jr. 1957. Centrifugal speciation. Q Rev Biol 32:247-277.

Callcott A-M, Collins HL. 1996. Invasion and range expansion of imported fire ants (Hymenoptera: Formicidae) in North America from 1918-1995. The Florida Entomologist 79:240-251.

Ross KG, Vargo EL, Keller L. 1996. Social evolution in a new environment: the case of introduced fire ants. Proc Nat Acad Sci USA 93:3021-3025. Abstract

Shoemaker DD, Ross KG, Arnold ML. 1996. Genetic structure and evolution of a fire ant hybrid zone. Evolution 50:1958-1976.

Tsutsui ND, Suarez AV. 2003. The colony structure and population biology of invasive ants. Conservation Biol 17:48-58. doi:10.1046/j.1523-1739.2003.02018.x

Wilson EO. 1953. Origin of the variation in the imported fire ant. Evolution 7:262-263.

I ran across this paper from a few years ago by John Avise and DeEtte Walker, which considers the implication of reticulation-based species concepts for mtDNA-generated phylogenies.

After quoting Dobzhansky on natural categories, they point to the central problem with using mtDNA phylogenies to define species: a clonally inherited gene does not easily lend itself to testing horizontal gene transfer:

In this same spirit, we ask here whether biotic discontinuities as seen through the eyes of laboratory-based mitochondrial geneticists tend to bear resemblance in number and composition to the biological units currently recognized as taxonomic species. There are additional reasons for interest in the outcome. First, discontinuities might be evident in local biotas (the nondimensional species perception) but may blur when geographic variation is taken into account. Molecular phylogeographic studies address this issue, because they explicitly analyze spatial variation (6, 7). Second, under the biological species concept (BSC), a sexual species usually is perceived as a reproductive community whose gene pool retains coherency primarily via the bonds of interbreeding and genetic exchange (1, 8); however, mtDNA molecules are transmitted asexually, and matrilines are nonreticulate. Thus, any genuine unities within (and discontinuities between) groups of organisms in mtDNA genotype cannot be attributed to "horizontal" patterns of contemporary lineage anastomosis via mating per se. Instead, they must be caused by "vertical" connections (and partitions) in matrilineal phylogenies. However, vertical connections themselves are functions of the demographic histories of population units demarcated by temporally extended patterns of interbreeding and gene flow.

I think this passage puts the situation more direly than deserved -- after all, every gene is vertically inherited. Mitochondrial DNA is no exception. It can be transferred by gene flow just as surely as any autosomal gene.

No, the key difference is that clonal inheritance leaves mtDNA with a greatly reduced effective size compared to autosomal (or X-linked) genes. This means that a given amount of gene flow is vastly less effective at dispersing mtDNA variants. Hence mtDNA (and Y chromosomes) have much higher F_ST (at equilibrium) than other genetic markers.

In other words, longstanding populations within a species will tend to look more divergent considering only their mitochondrial DNA than considering their autosomal genes. We can see this pattern when considering differences among subspecies of chimpanzees and other hominoids. The subspecies are highly distinct from each other considering only their mtDNA, with long divergence times ranging higher than a million years. The other uniparentally inherited genetic system, the nonrecombining portion of the Y chromosome (NRY) shows a similar pattern -- subspecies of chimpanzees are highly distinct, sharing no NRY lineages (Stone et al. 2001). In contrast, there is substantially more sharing of variants at autosomal sites (Fischer et al. 2004). Chimpanzee subspecies share many fewer autosomal variants than are shared among human groups, but they share many more autosomal than mtDNA or Y chromosome variants. Gorilla genes follow a similar pattern: mtDNA indicates very strong divergence between western and eastern gorillas, while autosomal genes show evidence for recurrent gene flow between them up to 150,000 years ago (Thalmann et al. 2007).
Avise and Walker compared mtDNA phylogenies for vertebrates with commonly accepted taxonomic species, finding roughly twice as many deep mtDNA phylogroups as taxonomic species. They consider that these generally represent historical patterns of demography and constrained gene flow within species.

Coalescent patterns in gene trees are related intimately to historical patterns in population demography (7, 21, 22). In particular, tight connections among nonanastomose [nonreticulating] genotypes suggest recent lineage coalescence to a shared ancestor, likely because of relatively small evolutionary effective population sizes that cause extant lineages to have shallow temporal depth. Conversely, large genetic gaps between gene-tree branches suggest long-standing historical population separations. In support of this likelihood, nearly all of the deep phylogenetic disjunctions registered in the intraspecific mtDNA gene trees in this review involved regionally separate populations.

This is basically saying that regional differentiation within species is an important source of genetic variability. They mention that male-mediated dispersal would create patterns not easily tested with mtDNA; this is one factor but broadly, any single gene will create a phylogeny that is potentially discordant with others in various ways.

References:

Avise JC, Walker D. 1999. Species realities and numbers in sexual vertebrates: Perspectives from an asexually transmitted genome. Proc Nat Acad Sci USA 96:992-995. Abstract

Fischer A, Wiebe V, Pääbo S, Przeworski M. 2004. Evidence for a complex demographic history of chimpanzees. Mol Biol Evol 21:799-808. doi:10.1093/molbev/msh083

Stone AC, Griffiths RC, Zegura SL, Hammer MF. 2002. High levels of Y-chromosome nucleotide diversity in the genus Pan. Proc Nat Acad Sci USA 99:43-48. doi:10.1073/pnas.012364999

Thalmann O, Fischer A, Lankester F, Pääbo S, Vigilant L. 2007. The complex evolutionary history of gorillas: insights from genomic data. Mol Biol Evol 24:146-158. doi:10.1093/molbev/msl160