Selection in males purges the mutation load on female fitness

Abstract

Theory predicts that the ability of selection and recombination to purge mutation load is enhanced if selection against deleterious genetic variants operates more strongly in males than females. However, direct empirical support for this tenet is limited, in part because traditional quantitative genetic approaches allow dominance and intermediate‐frequency polymorphisms to obscure the effects of the many rare and partially recessive deleterious alleles that make up the main part of a population's mutation load. Here, we exposed the partially recessive genetic load of a population of Callosobruchus maculatus seed beetles via successive generations of inbreeding, and quantified its effects by measuring heterosis—the increase in fitness experienced when masking the effects of deleterious alleles by heterozygosity—in a fully factorial sex‐specific diallel cross among 16 inbred strains. Competitive lifetime reproductive success (i.e., fitness) was measured in male and female outcrossed F1s as well as inbred parental “selfs,” and we estimated the 4 × 4 male‐female inbred‐outbred genetic covariance matrix for fitness using Bayesian Markov chain Monte Carlo simulations of a custom‐made general linear mixed effects model. We found that heterosis estimated independently in males and females was highly genetically correlated among strains, and that heterosis was strongly negatively genetically correlated to outbred male, but not female, fitness. This suggests that genetic variation for fitness in males, but not in females, reflects the amount of (partially) recessive deleterious alleles segregating at mutation‐selection balance in this population. The population's mutation load therefore has greater potential to be purged via selection in males. These findings contribute to our understanding of the prevalence of sexual reproduction in nature and the maintenance of genetic variation in fitness‐related traits.

The mating system affects the temperature sensitivity of male and female fertility

“…(b) Comparison of male and female TSF for the studies presented in panel a. Further details, including inclusion criteria for reviewed studies and a table of all values, are presented in Supporting Information Appendix S5and is more than three times as effective at purging deleterious alleles compared to fecundity selection on females under semi-natural laboratory setting, as used here (Grieshop et al, 2016(Grieshop et al, , 2021. One plausible mechanism behind the result is therefore that sexual selection in the polygamous mating regime led to more efficient purging of alleles with deleterious effects on male mating success, relative to purging of alleles with deleterious effects on female viability and fertility.…”

“…We first quantified how two generations of natural and sexual selection on artificially induced mutations affected short-term evolutionary responses in male and female TSF. This approach was motivated by (a) theory often assuming that sexual selection is a more potent force of purifying selection against deleterious genetic variation compared to natural selection (Rowe & Houle, 1996;Tomkins et al, 2004;Whitlock & Agrawal, 2009) and that purging of deleterious genetic variation is much more efficient via sexual selection in males in C. maculatus (Grieshop et al, 2016(Grieshop et al, , 2021, (b) the notion that compensatory physiological responses to temperature stress are costly (Feder et al, 2000), suggesting that TSF may be dependent on the condition and overall genetic quality of the individual, and (c) the observation that elevated temperature can increase the effects of deleterious genetic variation in ectotherms (Berger et al, 2021).…”

Direct and indirect effects of male genital elaboration in female seed beetles

“…That exaggerated sexually selected traits come to reflect the genetic quality of their bearer, through 'genic capture', is an essential assumption of the good genes process because it aligns male reproductive fitness with nonsexual fitness components [2,23]. This possibility is supported by the effects of induced deleterious mutations on reproductive fitness being to some extent shared between the sexes in seed beetles [57] and by the fact that the naturally occurring mutation load on fitness in male seed beetles is indeed negatively genetically associated with female fitness [34]. We note, however, that the strength of condition-dependent expression of genital spines is apparently variable (see above) and the relative importance of good gene effects is thus likely to vary across populations and environments in this species, a prediction underscored by the fact that the genetic correlation between male and female reproductive fitness is known to vary from positive to negative [58][59][60][61].…”

“…Therefore, it is reasonable to hypothesize that an evolutionary outcome of the sexually antagonistic evolution of these elaborate genitalia may involve a good genes process, where females gain indirect benefits from having their offspring fathered by males with elaborated genitalia. A recent study of seed beetles demonstrating that a high genetic load for reproductive fitness in males is genetically associated with low female lifetime offspring production [34] supports this possibility. Here, we assess the direct effects of the spines on female fitness and then ask whether exaggerated spines are genetically associated with indirect benefits to females.…”

The stagnation paradox: the ever-improving but (more or less) stationary population fitness

“…A mix of results, from negative to positive, is not wholly unexpected in a situation where theory shows sexual selection to have the potential to elevate female fitness. Beneficial effects at the genetic level arise because selection against deleterious genetic variants operates more strongly on sexually selected males than females [ 66 ]. In such a setting, the gene pool is purged without causing a large demographic cost on females, and such processes may be particularly important when both sexes are far away from the current fitness peak [ 67 , 68 ].…”