I read this paper in bed yesterday before going to sleep:
Presgraves and Yi, Trends in Ecology & Evolution 2009
Two patterns from large-scale DNA sequence data have been put forward as evidence that speciation between humans and chimpanzees was complex, involving hybridization and strong selection. First, divergence between humans and chimpanzees varies considerably across the autosomes. Second, divergence between humans and chimpanzees (but not gorillas) is markedly lower on the X chromosome. Here, we describe how simple speciation and neutral molecular evolution explain both patterns. In particular, the wide range in autosomal divergence is consistent with stochastic variation in coalescence times in the ancestral population; and the lower human–chimpanzee divergence on the X chromosome is consistent with species differences in the strength of male-biased mutation caused by differences in mating system. We also highlight two further patterns of divergence that are problematic for the complex speciation model. Our conclusions raise doubts about complex speciation between humans and chimpanzees.
Complex speciation between humans and chimpanzees
You might remember the Patterson et al. paper in Nature back in 2006, that argued for a complex speciation of humans and chimps: An early separation between the two, followed by a hybridization and then the extinction of one of the species ancestral to the hybrids.
The arguments for this theory were 1) large variation in divergence time along the autosomal chromosomes and 2) a much more recent divergence of the X chromosome compared to the autosomes.
Wakeley then argued that 1) at least didn’t need any complex speciation history. The variation in divergence is actually as would be expected just from variation in coalescence times along the chromosomes, assuming a reasonably large effective population size of the human/chimp ancestor species.
As for 2), the coalescence process alone cannot explain the recent divergence of X chromosomes. We do expect a more recent divergence of X chromosomes than autosomes, since the effective population size of X chromosomes is 3/4 of that of the autosomal chromosomes, but the divergence of the X chromosomes is less than what can be explained by this.
This could either be explained by selection on the X chromosome (which essentially reduces the effective population size and thus leads to a reduced divergence) or by the difference in mutation rate between males and females that would affect the X chromosome differently than the autosomes (reducing the difference between the two).
It is well known that there is a bias in mutation rate between males and females, having to do with the average number of genome replications per generation in males and females, respectively. The details I won’t go into here (although they are pretty important for the post, the post would just get too long and I don’t want to loose the readers who already know this … I might write about it in a separate post another day…)
Selection is probably not likely. It would require a pretty uniform selection across the X chromosome. The male-biased mutation explanation sounds more reasonable.
A problem with both explanation, though – Patterson et al. argued in their reply – is that this weird pattern in X is only observed between human and chimp and not between human and gorilla (or chimp and gorilla).
If mutation-rate differences alone could explain the observed data, we would expect a consistent value for from the human–chimpanzee and human–gorilla divergence data, but estimates of are significantly different (P = 0.001). A high value of also cannot explain other important features in Table 1: the near-absence of sites on chromosome X that cluster humans and gorillas or chimpanzees and gorillas; or why human–gorilla divergence should not be reduced on chromosome X (such a reduction would be expected if high male mutation rate were responsible for low human–chimpanzee genetic divergence on chromosome X).
Lineage specific male biased mutation rate
The Presgraves and Yi paper argues that male biased mutation rate can explain the pattern after all.
True, the low divergence on X is only observed between humans and chimps and not between humans and gorillas, but if the strength of this bias is larger on the human and chimp lineages than on the gorilla lineage it could still be an explanation.
Chimps are very promiscuous, humans somewhat less so, while gorillas are polygynous. This affects sperm production so chimps produce most sperm per ejaculation, gorillas the least and humans again inbetween.
With more sperm produced in humans and chimps than in gorillas, it is therefore conceivable that the mutation bias is stronger in chimps and humans than in gorillas.
So they estimate this bias per lineage and get exactly that result: the bias is strongest in chimps, intermediate in humans and weakest in gorillas:
With different male-biased mutation rate in the lineages, with much less bias in gorillas, there is nothing strange in a reduced divergence on X chromosomes between humans and chimps than between humans and gorillas.
Voilà! No more need for a complex speciation history!
At least until the next paper…
- Presgraves, D., & Yi, S. (2009). Doubts about complex speciation between humans and chimpanzees Trends in Ecology & Evolution DOI: 10.1016/j.tree.2009.04.007
- Patterson N, Richter DJ, Gnerre S, Lander ES, & Reich D (2006). Genetic evidence for complex speciation of humans and chimpanzees. Nature, 441 (7097), 1103-8 PMID: 16710306
- Wakeley J (2008). Complex speciation of humans and chimpanzees. Nature, 452 (7184) PMID: 18337768
- Patterson, N., Richter, D., Gnerre, S., Lander, E., & Reich, D. (2008). Patterson et al. reply Nature, 452 (7184) DOI: 10.1038/nature06806