Allele surfing vs. Positive Selection

Continental human populations have very high allele frequency differences in several loci. One explanation for this phenomenon is that after their arrival in new lands, humans underwent selection for alleles that were appropriate in the new environments. An alternative explanation is that the frequencies were due to allele surfing, a process in which a small subset of individuals at the frontier of the expansion expands and multiplies into previously unsettled territory, causing their particular alleles to increase in frequency there.

From the paper:

The survey of the HGDP database on human polymorphisms reveals that large allele frequency differences between continental regions are extremely common. Indeed as much as 30% of loci show very large allele frequency differences between continents. These differences are unlikely to have been created by positive selection, but are more likely the result of neutral demographic processes such as the surfing phenomenon. Because the erosion of large allele frequency differences by mutation is slow, even for large mutation rates, the surprisingly large number of strongly differentiated STR alleles also do not need to be explained by the action of positive selection. Africa and the Americas show a much larger extent of differentiation than Eurasia or East Asia, which is certainly due to changes in allele frequencies during the colonisation of the Eurasian and the American continents. Disentangling the effects of selection and neutral demographic processes on genome diversity remains an important challenge of future human evolution studies.

This is a serious challenge to the selectionist paradigm and should be answered by its proponents. I would say that, from now on, the "gold standard" of positive selection should be concrete evidence that the proposed selected alleles actually do something that could have been selected, e.g., lactase persistence, where allele frequency differences are combined with a specific trait, which in turn is correlated with a particular selective influence (milk consumption after weaning). Statistical inference of selection without a comprehensive explanation is no longer intellectually convincing.

For example, ASPM and MCPH1 are loci that generated a lot of excitement as selection targets due to their large inter-group frequency differences. However, followup work has not found any substantial associations between them and anything of value: Has ASPM been the target of recent selection?, ASPM, MCPH1, CDK5RAP and BRCA1 and general cognition, reading or language. Were they really selected, or did they ride the wave of human advance?

Annals of Human Genetics doi: 10.1111/j.1469-1809.2008.00489.x

Large Allele Frequency Differences between Human Continental Groups are more Likely to have Occurred by Drift During range Expansions than by Selection

T. Hofer et al.

Several studies have found strikingly different allele frequencies between continents. This has been mainly interpreted as being due to local adaptation. However, demographic factors can generate similar patterns. Namely, allelic surfing during a population range expansion may increase the frequency of alleles in newly colonised areas. In this study, we examined 772 STRs, 210 diallelic indels, and 2834 SNPs typed in 53 human populations worldwide under the HGDP-CEPH Diversity Panel to determine to which extent allele frequency differs among four regions (Africa, Eurasia, East Asia, and America). We find that large allele frequency differences between continents are surprisingly common, and that Africa and America show the largest number of loci with extreme frequency differences. Moreover, more STR alleles have increased rather than decreased in frequency outside Africa, as expected under allelic surfing. Finally, there is no relationship between the extent of allele frequency differences and proximity to genes, as would be expected under selection. We therefore conclude that most of the observed large allele frequency differences between continents result from demography rather than from positive selection.

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