Sex is a big deal. William Hamilton spent a significant part of his career on the topic, and the second volume of his collected papers, The Narrow Roads of Gene Land, is focused on this issue. Whenever I talk about sex in an evolutionary biological context one thing that always pops up is why males? In other words, why do so many complex organisms have a whole sex which does not bear offspring? Parthenogenetic lineages of organisms where females can reproduce asexually have double the per generation reproductive output as sexual lineages. And yet over evolutionary history it seems clear that in lineages where sexual and asexual species coexist, the latter are always novel derived lineages. In other words, asexual lineages have a high extinction rate. Sex, and more specifically males, must be good for something. What then?
One hypothesis is that males are good for purging genetic load via sexual selection. On a genetic level all individuals carry deleterious mutations, which they pass on to their offspring. But, because of sample variance in transmission, there will be a distribution of outcomes in any given set of offspring. By chance some individuals will exhibit a higher load of deleterious alleles, while others will carry fewer alleles. If this load is correlated to traits which are visible to the opposite sex, then excess load every generation can be purged through reproductive skew. In other words, one might envisage a situation of sexual selection-mutation balance, where de novo mutations introduced every generation are balanced against deleterious alleles purged from the population through selection of more fit males.
All good in theory. But is this empirically true? A new paper in Nature suggests it is. At least for the red flour beetle. The paper is titled Sexual selection protects against extinction. Recall that asexual lineages seem to be more likely to go extinct when one examines them with comparative phylogenetic methods (i.e., with in a clade asexual lineages are invariably young in evolutionary time scales, implying that they do not last long).
The adapted figure above shows the experimental results which support the proposition that sexual selection purge deleterious alleles. These experiments ran for ~10 years, and consisted of varying primary treatments which differed in terms of intensity of sexual selection in red flour beetles. In panel A you see a comparison between a male and female skewed sex ratios (9:1), red and blue lines respectively. In a male skewed ratio the males are competing for the attention of a few females, and in a female skewed ratio the situation is the reverse. To test for the fitness of the lineages the researchers took the outcomes of long term breeding in these scenarios (fixing the effective population sizes to be comparable) and then forced them to engage in sibling matings. This would “expose” deleterious recessive alleles because of the nature of inbreeding. As is evident above in the female skewed (blue) lineages there is a much quicker extinction rate as inbreeding begins to expose deleterious alleles in the recessive phenotype. In the second set of experiments the authors compared polyandrous (5 males to 1 female) and monogamous lineages. Again, you see that the polyandrous lineages are much more robust to inbreeding, suggesting that sexual selection driving reproductive skew correlated with mutational load is resulting in a lower population wide genetic load.
There are many arguments for why sex persists (though many of them do not seem to directly address the cost of males, since sexuality does not necessarily entail two different sexes where one does not bear offspring or produce eggs). I don’t think that sexual selection needs to be the explanation as such. Additionally, I think there is the problem that extremely skewed sex ratios as is the case above does not seem biologically plausible in many organisms. In big and slow breeding organisms, such as humans, extreme sex ratios are not typically common. It seems unlikely that sex is maintained purely through purging of deleterious alleles via a “good genes” model of sexual selection. But then to truly test this hypothesis it strikes me that some sequencing methodologies could be brought to bear. For example, do individuals with lower load have a higher realized reproductive fitness? This is entirely testable.
Citation: Lumley, Alyson J., et al. “Sexual selection protects against extinction.” Nature (2015).