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Let’s talk about sexual selection and Charles Darwin

Charles Darwin famously posited the origin of species through adaptation driven by natural selection. The theory of evolution as we understand it. But another of Darwin’s major ideas was that sexual selection was very important in driving diversity within species. More specifically Darwin thought that female choosiness was critical and explained why in species such as birds the males were so much more “showy.”

Sexual selection is a huge field of study, and it’s hard to deny that it is a real thing. But, there has long been an argument about the efficacy of sexual selection within humans. Depending on how you define it, it does not seem that humans are particularly sexually dimorphic compared to common chimpanzees and gorillas, for example. This goes back to whether we are polygynous or monogamous. Because of high reproductive variation for males in polygyny sexual selection can drive changes really fast (e.g., one super-fit male can produce huge numbers of offspring). The situation in monogamy is more difficult since there is less reproductive variance.

A new preprint seems to suggest that selection is happening on males, even today, due to deleterious genes. Sex-biased reduction in reproductive success drives selective constraint on human genes:

Genome-wide sequencing of human populations has revealed substantial variation among genes in the intensity of purifying selection acting on damaging genetic variants. While genes under the strongest selective constraint are highly enriched for Mendelian disorders, most of these genes are not associated with disease and therefore the nature of the selection acting on them is not known. Here we show that genetic variants that damage these genes reduce reproductive success substantially in males but much less so in females. We present evidence that this reduction is mediated by cognitive and behavioural traits, which renders male carriers of such variants less likely to find mating partners. Our findings represent strong genetic evidence that Darwin’s theory of sexual selection is shaping the gene pool of contemporary human populations. Furthermore, our results suggest that sexual selection can account for about a quarter of all purifying selection acting on human genes.

The figure to the right gets at the major finding. More mutations mean a far more rapid drop in fitness for males than females. Why? The major reason seems to be that males can’t find a partner. If they can find a partner, the effect is much weaker. Basically, this is detecting an increase in childlessness.

A plausible explanation is that it impacts fertility, but the above indicates that that is not the case. And, the deleterious mutations aren’t enriched in the testes, nor does pruning out loci with known reproductive effects remove the impact. The authors also looked at intelligence. Those with mutations were not as intelligent, but that can’t explain most of the effect (and obviously it didn’t have much of an impact on women). The same with known conditions such as schizophrenia. Rather, what’s going on is that people are picking up on overall “genetic quality.”

There are major limitations of course. This is in British people. And, the samples from the Biobank tend to be somewhat healthier than average. There is a lot more work to be done with a lot more samples. But this is an awesome result in that it synthesizes the power and methods of modern genomics with a classical evolutionary hypothesis about the shape of human variation.

The main question I have regarding sexual selection then is what will the results in other societies be? As per Joe Henrich’s recent book, The WEIRDEST People in the World, the British have been in enforced monogamy for 1,000 years. Purifying selection could be much stronger in some non-WEIRD societies (and in inbred Arab cultures cousin-marriage would also ‘expose’ recessive alleles faster). That might mean there aren’t as many deleterious alleles. Or, it could be the effect is much stronger in those who have no children (males).

This is just the beginning. Perhaps it’s time to reread Geoffrey Miller’s The Mating Mind?

5 thoughts on “Let’s talk about sexual selection and Charles Darwin

  1. Hmmm. “Genetic quality” – Could quickly take on a very euphemistic meaning. England has been rather unique in the degree of monogamous coupling for the past 1000 years.
    Based on prior surname studies and primogeniture inheritance patterns it could be argued there has been greater male selection pressure in the UK. Those studies show for most of the period there was later average marriage age and first child birth than the rest of Europe. Church records show the cascade of family names from well born down to penniless in 2-3 generations. The norm was for under resourced females/males not to marry or have children.
    The constant “washing out” of younger sons might explain these results. The usual caveat – further studies required – applies.

  2. “That might mean there aren’t as many deleterious alleles. Or, it could be the effect is much stronger in those who have no children (males)”

    Both the cases would be very strong. Marrying in the same family/ cousin would lead to sterile males in few generation.
    Deleterious alleles can be carried in small community at much higher rate. Eg Turner syndrome/ Noonan symptoms can be carried in higher frequency.

  3. Q: Does this get us any closer to testing the contraversy over whether female choice driven sexual selection acted at all in humans? The counterargument by blogger Evolving_Moloch is that human reproductive tended to be arranged and governed by kin networks, mostly with older males in charge of these. So selection hit men, but not so much *sexual* selection. Is there anything more or less consistent with this in this data?

    Another comment on – “the British have been in enforced monogamy for 1,000 years – true, but from what I have heard of the history, in contrast with Asia, this also came with larger fractions of men and women who did not reproduce at all (late and non-universal marriage, per Malthus and Allen and all that) as IslandView notes, and with weaker family networks arranging marriages for kin. Those might expose mutations a bit more.

  4. @IslandView, though “second sons” shouldn’t be any less fit (or genetically different, on average) than “first sons”, so that seems like it wouldn’t be linked to a selective effect? It has to be some effect where fitness is getting exposed, not dispersal of parental resources in a way that’s randomly distributed with effect to fitness (e.g. sometimes the “fit” elder son inherits and “unfit” younger son does not, sometimes the “unfit” elder son inherits and “fit” younger son does not, and it all averages out to nothing).

    Another more general comment about the ideas of non-universal marriage is, I guess, would be that we probably can’t naively assume that the any individuals who failed to marry would have equal fitness, under a cultural regime where marriage was universal/arranged.

    The paper describes “cognitive and behavioural factors (which could decrease ability to find a mate, or increase voluntary childlessness)”. It seems kind of unlikely that a male who failed to find a mate under one sort of society would necessarily be able to have as many surviving children if that was solved under another sort of society, while voluntary childlessness could occur under both “marital regimes”.

    Another thing is; OK paper suggests not linked to fertility (no expression in testes!), but does that necessarily mean linked to cognitive / behavioural traits? Males have lots of traits that affect fitness that are non-cog. / non-behav. Physical appearance, work capacity.

  5. Razib says: “in inbred Arab cultures cousin-marriage would also ‘expose’ recessive alleles faster”

    Interesting point. I always thought inbreeding=bad, but Razib points out that inbreeding + selection=expression and subsequent elimination of (deleterious) recessive alleles.

    I guess the Hapsburgs and Egyption Pharoahs didn’t have enough selection effect happening.

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