The Impact Of Polygyny On Human Genetic Variation

This morning Dienekes pointed out a new paper in the open access journal PLoS Genetics on polygyny and its impact on human genetic variation. Razib followed suite, providing a more in depth review of the study. I recommend you check out both. In this post, I’m also gonna have a stab at reviewing the paper since it has an important anthropological impact.

The paper, “Sex-Biased Evolutionary Forces Shape Genomic Patterns of Human Diversity,” is authored by some people you may have heard of, such as Michael Hammer and Jeffrey Wall among others. Like many population geneticists, they isolated the problems and limitations of previous studies which investigated genetic diversity of humans from only markers on the mitochondrial DNA and non-recombining portion of the Y chromosome genome. They proposed that markers on the autosomal genome, including the X sex chromosome, will provide a more insightful understanding.

So they compared the genetic variation among 40 independent loci on the X chromosome and autosomes in 90 individuals from six different populations. 20 loci on the X chromosome and 20 on the autosomes were picked from non-coding regions of the genome.

Why wasn’t there a more even distribution of sites across the whole genome? Well, the authors specifically sought to seek out the impact of sex-specific processes, such as mating patterns, in shaping genomic patterns of variability. Both Razib and Dienekes do an excellent job in explaining this, but I’ll snip what Razib wrote since it is more clear in my mind:

“Assuming equal numbers of males and females in any given generation you expected a ratio of diversity of 0.75 between the X and the autosomes; remember that the number of copies of X circulating within the population are reduced by 25% because males carry only one copy, while women carry two.”

In other words, the X chromosome is present in two copies in females and a single copy in males. We all know that. We expect that the other chromosomes will show more genetic diversity than the X chromosome in a population with an equal number of breeding males and females because they are inherited equally by both sexes from each parent. In a populations with an unequal number of breeding males to females, we should see something different. Actually, we expect to see more genetic diversity on the X chromosome than on the other chromosomes in areas where men don’t get to pass on their genes, while most women do.

The authors’ samples included individuals from Africa, such as the Biaka of the Central African Republic, the Mandenka from Senegal, and the San from Namibia were included. Outside of Africa, the French Basque, the Han Chinese and Melanesians were also sampled. Roughly 210kb of DNA was sequenced from each of these individuals, and a basic statistical summary of the nucleotide diversity in six human populations was conducted. Comparing the observed nucleotide diversity on the X chromosome to the chromosomes showed that there was more genetic differences in the X chromosome than would be expected if equal numbers of males and females tended to mate.

Even though I explained this in two paragraphs above, polygyny could be the only reason why we see such results. Some men just didn’t get a chance to pass on their genes. The authors even made sure to rule out background selection, changes in population size and sex-specific migration in their conclusion. Only the process of polygyny could account for the sex ratio skew and resulting patterns of genomic variation. By this process, fewer unique male genes are being passed into the next generation.

In the same issue, a very similar paper was also published that I don’t think many other people noticed. A separate team of academics applied this multilocus approach to the genetic diversity of Central Asia. It is published under the title, “Sex-Specific Genetic Structure and Social Organization in Central Asia: Insights from a Multi-Locus Study.” Their sample included 10 populations of bilineal agriculturalists and 11 populations of patrilineal herders from West Uzbekistan to East Kyrgyzstan. Bilineal means that there’s an even migration of men and women while patrilineal means there’s an uneven migration of women to their husband’s location. In total, their sample size represents 780 healthy adult men from 5 ethnic groups: Tajiks, Kyrgyz, Karakalpaks, Kazaks, and Turkmen. They conclude that the number of reproductive individuals is likely to be higher for women among patrilineal populations.

Both these studies show that the organization and structure of patrilineal populations is the likely cause of the observed genetic patterns, where men tend to father children with more females than females do with males despite institutionalized monogamy.

    Michael F. Hammer, Fernando L. Mendez, Murray P. Cox, August E. Woerner, Jeffrey D. Wall, Dmitri A. Petrov (2008). Sex-Biased Evolutionary Forces Shape Genomic Patterns of Human Diversity PLoS Genetics, 4 (9) DOI: 10.1371/journal.pgen.1000202
    Laure Ségurel, Begoña Martínez-Cruz, Lluis Quintana-Murci, Patricia Balaresque, Myriam Georges, Tatiana Hegay, Almaz Aldashev, Firuza Nasyrova, Mark A. Jobling, Evelyne Heyer, Renaud Vitalis, Molly Przeworski (2008). Sex-Specific Genetic Structure and Social Organization in Central Asia: Insights from a Multi-Locus Study PLoS Genetics, 4 (9) DOI: 10.1371/journal.pgen.1000200

6 thoughts on “The Impact Of Polygyny On Human Genetic Variation

  1. Interesting. I have often had some trouble with genetic studies of human populations in prehistory since they seldom take complicated factors such as continual intermarriage across ethnic groups, kinship systems, or adultery/rape/prostitution into account IMO.

    Question: Some modern studies have shown that a lot of children do not have the father their mother claim. of course, in a repressive patriarchal system adultery by married women tends to be less but do researchers take into account that there are a lot of offspring produced ‘on the wrong side of the marital bed’? Is it only institutional polygyny, or married women taking lovers their husband do not knpw about?

  2. I also have the same question. We know that Melanesians tend to be polygynic (I’m thinking of Papuans specifically) but the other high “polygyny” group are Northern Basques (the only European pop. sampled) and there is no record of Basques practicing polygamy at all (instead the monogamic household is a national institution).

    Humboldt instead mentioned in the early 19th century that pre-marriage promiscuity was common amon Basques and that marriages often happened when the girl became pregnant (not necesarily of her primary boyfriend, but hard to know). We know also that deeper in the past (as late as the 16th century) Basques practiced pagan or “witchcraft” ceremonies that were pretty much orgiastic (community sex on friday night under the influence of drugs, possibly stramonium).

    So I do suspect that this “polygynic” reproductive bias can be achieved by very different means: either by the typical patriarchal “harem” or by the less obvious women-led selection of prefered fathers in a relatively promiscuous context.

    The lowest level of “polygynic” bias was shown, maybe meaningfully, by the only hunter-gatherer sample: the Bushmen (San), who do not appear (AFAIK) to be either polygamous nor particularly promiscuous.

  3. Oops… the Biaka (Pygmies) are also hunter-gatherers and they show a more average “polygynistic” trend (almost as high as the Han and Mandenka). Still hunter-gatherers appear to show the lower levels of this trend overall.

  4. Is it possible that there a selective advantage to alternating periods of polygenic matings and offspring to provide fathers with presumably better phenotypes; and THEN the social group reverts to monogynic reproduction to avoid consaguinity?

    IF so then the open and legal monogamy and polygyny of countries where polygamy is legal today might be better statistical studies than the children of modern “Edens.”

  5. I have been thinking about this for a while and this topic is a part my research project. I cannot believe that polygyny had that big effect to make big difference in effective population size between male and female. I always believed that variance in reproductive success due to polygyny is not that big among human, because compared to monogamous males, only a few males (very rich men, maybe) successfully had multiple wives and significantly more children who survive until their reproductive age to reproduce more children. Some males have more children, but it does not means their children survive until their reproductive age to reproduce. Contrary to the authors of the article (Hammer and his colleagues), I think female gene flow was more important factor influencing X chromosome and mtDNA variation. What do you guys think? Does anybody have comment on this?

  6. Now, there are at least two groups of researchers challenge Hammer’s view and they view that polygyny was not an important factor in human evolutionary history influencing genetic variation. In fact, Hammer and his colleagues say that, in addition to the practice of polygyny, other polygynous processes (not clear what they are) and other demographic factors can also explain the observed pattern of female-to-male effective population size ratio. Hammer and his colleagues also considered how female gene flow affected the ratio, but they did not consider this thoroughly.

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