The (non-)neutral Neandertals

OK, I'm clearly going to have to cut out the beer if I'm going to do anything about stories like this one:

New research led by UC Davis anthropologist Tim Weaver adds to the evidence that chance, rather than natural selection, best explains why the skulls of modern humans and ancient Neanderthals evolved differently. The findings may alter how anthropologists think about human evolution.
Weaver's study appears in the March 17 issue of the Proceedings of the National Academy of Sciences. It builds on findings from a study he and his colleagues published last year in the Journal of Human Evolution, in which the team compared cranial measurements of 2,524 modern human skulls and 20 Neanderthal specimens. The researchers concluded that random genetic change, or genetic drift, most likely account for the cranial differences.
In their new study, Weaver and his colleagues crunched their fossil data using sophisticated mathematical models -- and calculated that Neanderthals and modern humans split about 370,000 years ago. The estimate is very close to estimates derived by other researchers who have dated the split based on clues from ancient Neanderthal and modern-day human DNA sequences.
The close correlation of the two estimates -- one based on studying bones, one based on studying genes -- demonstrates that the fossil record and analyses of DNA sequences give a consistent picture of human evolution during this time period.
"A take-home message may be that we should reconsider the idea that all morphological (physical) changes are due to natural selection, and instead consider that some of them may be due to genetic drift," Weaver said. "This may have interesting implications for our understanding of human evolution."

If you've been reading for long, you might reasonably wonder what I think about this study. My work has shown rapid natural selection in recent humans, consistent with evidence from recent skeletal samples for rapid evolutionary change. So it might seem incongruous that a study could assume that there has been no natural selection on the skeletal traits of recent human populations, and come to any kind of sensible conclusion.

I am actively working on this particular problem, with a manuscript in preparation, so I don't want to comment too extensively. However, I can say a brief word about why I disagree with the analysis.

A model of phenotypic evolution by genetic drift requires an assumption about the effective size of the population (Ne). Weaver et al. (2008) assume a model of "mutation-drift equilibrium." This is an assumption that the effective population size has not changed over time in the populations under consideration -- in this case, the Neandertal and human populations back at least as far as their common ancestor.

In their analysis, Weaver et al. (2008:4647) assume that the effective sizes of the human and Neandertal lineages, throughout the last few hundred thousand years, were equal to 2700 individuals. They wrote this:

The second reference point is the effective population size, PNe, under a mutation-drift-equilibrium model for sub-Saharan African human populations. Zhivotovsky and colleagues (ref. 17) estimated Ne from 271 microsatellites using an equation equivalent to our Eq. 7 as ≈ 2,700 individuals. Once again, we are just assuming that the morphological and microsatellite estimates should match up under the same model, not that this is the most realistic model to use to infer the actual effective population size.

This is an astounding assumption. It is important because a small effective size allows rapid evolution by genetic drift. But it is contradicted by other evidence.

For one thing, most other sets of genetic data indicate a long-term effective size of at least 10,000 for human populations -- four times larger than assumed in this study. All things being equal, this means that the rate of phenotypic evolution by genetic drift should be four times slower than assumed by Weaver et al. (2008). Some of this difference between real and assumed effective sizes may be washed out by their process of calibration -- their equations involve several unknowns that must be simultaneously estimated, and give a lot of wiggle-room to the results. But that points to another weakness of the analysis -- there's so much wiggle room that almost any level of phenotypic difference might look like "drift."

Moreover, the human population has vastly increased in numbers within the last 50,000 years. Weaver et al. (2008) use the phenotypic and genetic divergences of recent humans to calibrate their "clock" of phenotypic evolution. But the phenotypic divergences between recent human populations, with very large effective population sizes (Ne > 100,000) are simply not comparable to those between Middle Pleistocene humans and Neandertals -- at least, not without taking into account the vast difference in effective population sizes.

But please don't take my word for it. I am a clear partisan on the side of natural selection in recent human evolution. Weaver's quote in the press release above implies that we should accept a pluralistic model, in which genetic drift accounts for some changes. I agree entirely. But their analysis assumes that genetic drift accounts for all changes. I don't deny the role of genetic drift, but I do deny that it explains much about recent skeletal evolution in humans. Random chance cannot do much in a very large population in a few hundred generations.

I really don't understand why you would want to use a heuristic value for effective population size, when it is contradicted by genetic and archaeological evidence. I will be writing about effective population size over the next week, introducing some of the importance of the concept for these kinds of analyses. You're welcome to take a look at what I have to say, and take it or leave it.