Polygyny and X-chromosome diversity

Last year, a team of University of Arizona researchers found evidence of widespread polygyny in five different human populations: Biaka (Central African Republic), Mandenka (Senegal), San (Namibia), Basques (France), Han (China), and Melanesians (Papua New Guinea). In short, the maternally inherited X chromosome was genetically more diverse than the chromosomes inherited by both sexes (autosomes) (Hammer et al., 2008). So more women than men seem to have contributed to the gene pool. Surprisingly, there was little difference in this respect between the Mandenka (known to be highly polygynous) and the Basques and the Han (among whom the incidence of polygyny is much lower).

I was frankly skeptical. For one thing, maternally inherited genetic diversity reflects not only the number of women who contribute to the gene pool but also their own genetic diversity. If these women are drawn from a larger geographic area than the men are, the female gene pool will be more genetically diverse than the male gene pool. This is often the case. In a patriarchal society, land ownership is vested in the man’s lineage, so women are usually the ones who move to their mate’s community when they get married. We see this ‘patrilocality’ even in societies where land ownership is matrilineal. Among the Iroquois, wives were often abducted from other tribes through warfare.

In any case, the above findings have now been challenged. Another study has found much less maternally inherited genetic diversity in East Asians and Europeans than in West Africans (Keinan et al., 2008).

So what gives? The methodology is similar in both studies. John Hawks points out that the second study scales X-chromosome diversity to the human-macaque divergence whereas the first study uses the human-orangutan divergence. While this might explain differences in calculation of mutation rate and hence X-chromosome diversity, I don’t see how it could explain why one study found geographic differences (i.e., African versus non-African) and the other did not.

I suspect that the key difference is that the first study just did not have enough resolution to pick out these geographic differences, i.e., its dataset was too small. The second study used 130,000 loci (SNPs) whereas the first one used 40.


Please check out my latest article: “Sexual selection and human geographic variation” in The Journal of Social, Evolutionary & Cultural Psychology.

References

Frost, P. (2008). Sexual selection and human geographic variation, Special Issue: Proceedings of the 2nd Annual Meeting of the NorthEastern Evolutionary Psychology Society. Journal of Social, Evolutionary, and Cultural Psychology, 2(4), pp. 169-191.
http://www.jsecjournal.com/articles/volume2/issue4/NEEPSfrost.pdf

Hammer, M.F., Mendez, F.L., Cox, M.P., Woerner, A.E., & Wall, J.D. (2008). Sex-biased evolutionary forces shape genomic patterns of human diversity. PLoS Genet, 4(9), e1000202. doi:10.1371/journal.pgen.1000202

Keinan, A., Mullikin, J.C., Patterson, N., & Reich, D. (2008). Accelerated genetic drift on chromosome X during the human dispersal out of Africa. Nature Genetics, early view December 2008; doi:10.1038/ng.303

Polygyny or patrilocality?

Have all humans been more or less equally polygynous? The answer seems to be yes if we believe a team of researchers from the University of Arizona. They found that genetic diversity is higher on the maternally inherited X chromosome than on chromosomes inherited by both sexes (autosomes) in samples from five different populations: Biaka (Central African Republic), Mandenka (Senegal), San (Namibia), Basques (France), Han (China), and Melanesians (Papua New Guinea). Their conclusion: “our results point to a systematic difference between the sexes in the variance in reproductive success; namely, the widespread effects of polygyny in human populations.” In other words, proportionately more women than men have been contributing to the gene pool (Hammer et al., 2008).

It’s no surprise that polygyny has existed in the five populations under study. Almost all human populations are polygynous to some degree. The surprise is the relative lack of difference between the European and African subjects. Indeed, according to this study, the Basques have been more polygynous than the Mandenka have been. This is truly counterintuitive. Among the Basques, polygyny is normally limited to its serial form (marriage to a second wife upon the death of the first), as well as occasional cuckoldry. Among the Mandenka, polygyny is the preferred marriage type.

For some people in the blogosphere, this is simply scientific truth and we just have to accept it, however counterintuitive it may seem. There is nonetheless an alternate explanation: patrilocality. In many societies, a wife goes to live in her husband’s community after marriage. This has the effect of inflating the genetic diversity of women in any one community.

These two confounding levels of explanation, polygyny and patrilocality, bedeviled the previous methodology of comparing maternally inherited mtDNA with the paternally inherited Y chromosome. With the new methodology, patrilocality biases the results even more because the Y chromosome is no longer a point of reference.

The University of Arizona researchers do not mention patrilocality in their paper although they do discuss ‘sex-biased forces.’ Under this heading, they tested a model where only females migrate between communities (‘demes’) and at such a rate that panmixia eventually results. They concluded that this factor could not be significant. To my mind, the model is unrealistic, partly because the assumed migration rate is far too high and partly because two demes are used to represent a real world where brides are exchanged among many communities separated by varying genetic distances. To be specific, the more genetically different a bride is from her host community, the further away will be her community of origin, and the lower will be the probability of panmixia between the two.

To the extent that the methodology is biased toward patrilocality effects, any polygyny effects will be less apparent. If this new methodology primarily tracks differences in patrilocality, no major differences would be observable among the different population samples.

In addition, there may be a weak inverse relationship between patrilocality and polygyny. Patrilocality correlates with patriarchy, which correlates with high paternal investment, which inversely correlates with polygyny. If so, the two effects – polygyny and patrilocality – would tend to cancel each other out in the data.

Finally, the burden of proof is on those who propose new methodologies, especially one that produces inconsistent results. The University of Arizona researchers themselves say as much: “Our findings of high levels of diversity on the X chromosome relative to the autosomes are in marked contrast to results of previous studies in a wide range of species including humans.” More importantly, their findings run counter to the comparative literature on human mating systems. To cite only one authority, Pebley and Mbugua (1989) note:

In non-African societies in which polygyny is, or was, socially permissible, only a relatively small fraction of the population is in polygynous marriages. Chamie's (1986) analysis of data for Arab Muslim countries between the 1950s and 1980s shows that only 5 to 12 percent of men in these countries have more than one wife. … Smith and Kunz (1976) report that less than 10 percent of nineteenth-century American Mormon husbands were polygynists. By contrast, throughout most of southern West Africa and western Central Africa, as many as 20 to 50 percent of married men have more than one wife … The frequency is somewhat lower in East and South Africa, although 15 to 30 percent of husbands are reported to be polygynists in Kenya and Tanzania.

References

Hammer, M.F., Mendez, F.L., Cox, M.P., Woerner, A.E., & Wall, J.D. (2008). Sex-biased evolutionary forces shape genomic patterns of human diversity. PLoS Genet, 4(9), e1000202. doi:10.1371/journal.pgen.1000202

Pebley, A. R., & Mbugua, W. (1989). Polygyny and Fertility in Sub-Saharan Africa. In R. J. Lesthaeghe (ed.), Reproduction and Social Organization in Sub-Saharan Africa, Berkeley: University of California Press, pp. 338-364.