Mutation rates may be explained by differences in female promiscuity.
A genetic analysis has called into question the controversial claim that early humans and chimpanzees interbred before splitting into separate species.
"Many evolutionary biologists were pretty sceptical" about the interbreeding scenario, says evolutionary geneticist Soojin Yi of the Georgia Institute of Technology in Atlanta. She argues that her explanation — which stems from promiscuity differences among primate species — is "simpler and hence more likely".
In 2006, David Reich and his colleagues at the Broad Institute in Cambridge, Massachusetts, compared the genomes of humans, chimps and three other primate species, and found that the separation of ancient humans from our closest cousins was more complex than a clean break. The time from the beginning to the completion of human-chimp divergence ranged over more than four million years across different parts of the genome, and the X chromosome seemed youngest of all, they reported in Nature1. The authors argued that there were in fact two splits — an initial divide, followed by interbreeding, and then final separation in which only a young X chromosome was retained.
Many researchers took issue with this interpretation, arguing that large ancestral population sizes could explain the wide range in genetic divergence times, so there was no need to invoke a complex speciation process. But these critiques still could not account for the youth of the X chromosome.
Now Yi, together with Daven Presgraves of the University of Rochester in New York, have reanalysed the data and suggest that species differences in the levels of female promiscuity can account for the chromosomal inconsistency. The original hypothesis is "way more of a headache for evolutionary biologists", says Yi. The data "can also be explained very well by well-established ideas in molecular evolution".
Males competing for mates produce different amounts of sperm depending on the mating habits of the species. Chimps are highly promiscuous, humans less so and gorillas not much at all. As such, male chimps face the stiffest competition, so they have the highest sperm counts and the largest testes of the three species. That means that they also undergo more rounds of sperm cell division and make more DNA copying mistakes, leading to higher mutation rates in males than in females. Reich and others had assumed that all primates had the same mutation bias, but Yi and Presgraves argue that mating relationships should be taken into account.
Because females have two X chromosomes and males have only one, the X spends more of its evolutionary history in females, whereas non-sex chromosomes split their time evenly between each gender. Thus, a male-biased mutation rate will lead to proportionally fewer genetic changes on the X and will seem to be younger when using a molecular clock, even if all the chromosomes diverged at around the same time, the researchers argue. Complex speciation is therefore unlikely to be the cause, they report in an invited opinion article in the October issue of Trends in Ecology & Evolution2.
"This elegant and simple explanation will be the last piece of the puzzle," says Hideki Innan, a population geneticist at the Graduate University for Advanced Studies in Kanagawa, Japan.
The X factor
But Reich is not convinced. Yi and Presgraves' model "is an exciting hypothesis, but it simply can't explain the data", he says. Their model predicts that chimps should continue to accumulate more mutations on the autosomes compared to the X chromosome even after the species split. But even when Reich reanalysed 30 times more sequence data than his team considered in the original paper, he could not find any difference between the human and chimp lineages.
What's more, only the double-split scenario could explain why genes shared by humans and gorillas, but not chimps, are found everywhere on the non-sex chromosomes but are largely absent on the X. Complex speciation "remains a far-out hypothesis", admits Reich. "But no one has come up with an alternative explanation for the data that holds water."
Presgraves counters that when he included orang-utan data in the analysis, he found that humans and chimps had similarly strong male-biased mutation rates, so he wouldn't expect differences between the two species. What matters, he says, is that both species are more biased than gorilla, which makes the divergence seem younger than when compared to the older primates. In addition, he says, humans share genes with gorillas — albeit at lower levels — which is consistent with his expectations.
Nicholas Barton, an evolutionary geneticist at the Institute of Science and Technology Austria in Klosterneuburg, says that the new theory has the advantage that it is testable. Researchers can survey more species to confirm whether male-biased mutation rates vary with sperm competition. Reich's idea, however, cannot be disproved.
Indeed, in 2003, Hans Ellegren, an evolutionary biologist at Uppsala University in Sweden, calculated the mutation bias in 31 bird species, and found that those with higher rates of extrapair paternity also had higher male mutation rates3.
Yi concedes that she can't definitively invalidate Reich's model. "Proof is very hard to come by in evolution biology, unfortunately," she says.
Chimps are more promiscuous than humans and thus may have higher mutation rates in their males' DNA.
Patterson, N., Richter, D. J., Gnerre, S., Lander, E. S. & Reiche, D. Nature 441, 1103-1108 (2006).
Presgraves, D. C. & Yi, S. V. Trends Ecol. Evol. advance online publication doi:10.1016/j.tree.2009.04.007 (2009).
Bartosch-Härlid, A., Berlin, S., Smith, N. G., Møller, A. P. & Ellegren, H. Evolution 57, 2398-2406 (2003).
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Dolgin, E. Human-chimp interbreeding challenged. Nature (2009). https://doi.org/10.1038/news.2009.870