Sexual selection on spontaneous mutations strengthens the between‐sex genetic correlation for fitness

Abstract

A proposed benefit to sexual selection is that it promotes purging of deleterious mutations from populations. For this benefit to be realized, sexual selection, which is usually stronger on males, must purge mutations deleterious to both sexes. Here, we experimentally test the hypothesis that sexual selection on males purges deleterious mutations that affect both male and female fitness. We measured male and female fitness in two panels of spontaneous mutation-accumulation lines of the fly, Drosophila serrata, each established from a common ancestor. One panel of mutation accumulation lines limited both natural and sexual selection (LS lines), whereas the other panel limited natural selection, but allowed sexual selection to operate (SS lines). Although mutation accumulation caused a significant reduction in male and female fitness in both the LS and SS lines, sexual selection had no detectable effect on the extent of the fitness reduction. Similarly, despite evidence of mutational variance for fitness in males and females of both treatments, sexual selection had no significant impact on the amount of mutational genetic variance for fitness. However, sexual selection did reshape the between-sex correlation for fitness: significantly strengthening it in the SS lines. After 25 generations, the between-sex correlation for fitness was positive but considerably less than one in the LS lines, suggesting that, although most mutations had sexually concordant fitness effects, sex-limited, and/or sex-biased mutations contributed substantially to the mutational variance. In the SS lines this correlation was strong and could not be distinguished from unity. Individual-based simulations that mimick the experimental setup reveal two conditions that may drive our results: (1) a modest-to-large fraction of mutations have sex-limited (or highly sex-biased) fitness effects, and (2) the average fitness effect of sex-limited mutations is larger than the average fitness effect of mutations that affect both sexes similarly.

Lineages evolved under stronger sexual selection show superior ability to invade conspecific competitor populations

“…In a mutation accumulation study with D. serrata , sexual selection did not prevent fitness reductions associated with the buildup of load, but did strengthen the fitness correlation between males and females, indicating an importance for sex‐limited genetic load for population fitness (Allen et al. ). Evidence that sexual selection helps to fix beneficial alleles more effectively when environments change also varies, with some studies reporting that sexual selection improves adaptation to a novel environment (Fricke and Arnqvist ), aids the evolution of pesticide resistance (Jacomb et al.…”

Genetic Quality Affects the Rate of Male and Female Reproductive Aging Differently in Drosophila melanogaster

“…This may at first appear as if our manipulation of genetic quality had a larger influence on condition in males. Instead, we attribute this larger difference in males to them experiencing stronger sexual selection-a compelling argument, as this effect is believed to be behind the stronger selection against deleterious mutations commonly observed in males compared to females (Whitlock and Agrawal 2009;Sharp and Agrawal 2013;Grieshop et al 2016; but see Allen et al 2017;Prokop et al 2017). An alternative explanation for this pattern is that D. melanogaster males have more sex-limited transcripts than do females overall, as the testes are particularly enriched for sex-limited gene expression (Graveley et al 2011).…”

Sexual dimorphism and sex-biased gene expression in an egg parasitoid species, Anastatus disparis

“…In contrast, studies in Tribolium castaneum and Anopheles gambiae [13] [14] have shown that many of the sex-biased genes in these species are female biased. In general, male-biased genes evolve more rapidly than female-biased genes [15] [16] [17] [18], suggesting that males experience stronger positive selection than females [4][5], although the genetic architecture of gene expression and other factors might also explain the more rapid evolution of male-biased genes [19]. Sex-biased gene expression has been documented in a range of different species, including brown algae [20], birds [21] [22], nematodes [23], Daphnia pulex [10], cichlid shes [24], guppies [25], moths [26], the pea aphid [27], and multiple insect species [8] [33].…”