Selection in males purges the standing genetic 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 populations 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 4x4 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 populations 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. Impact statementWhy do the large majority of eukaryotic species reproduce sexually if it means that females must spend half of their reproductive effort producing males, while males contribute few or no resources to offspring production themselves? In principle, a lineage of a mutant asexual female that simply clones herself into daughters would grow at twice the rate of her sexual competitors (all else equal). What prevents this from being the predominant mode of reproduction throughout eukaryotes? One hypothesis regards the role of males in facilitating the purging of deleterious mutations from the populations genome since very strong selection in males, unlike selection in females, can occur in many species without reductions in population offspring numbers. Due to the inherent difficulties of isolating this source of standing genetic variation for fitness, empirical evidence for this theory is mixed and limited to indirect evidence from manipulative experiments and experimental evolution studies. Here we demonstrate that recessive deleterious alleles in a population of the seed beetle, Callosobruchus maculatus, are selected against strongly in males but not females. Using a fully factorial diallel cross among 16 inbred strains, we measured the degree to which fitness in the outbred offspring of those crosses improved relative to their inbred parents. This measure is known as heterosis and offers an estimate of the relative amount of partially recessive deleterious alleles carried by a genetic strain. We then analyzed the relationship between the strains heterosis values and their additive genetic breeding values for fitness measured in males and females, revealing the extent to which segregating (partially recessive) deleterious alleles are selected against in males and females. We found that a strains heterosis value was strongly genetically correlated with its additive genetic breeding value for male fitness, but not female fitness. This suggests that mutations with deleterious effects on population growth rate due to their effects on females can be selected against (i.e. purged) more efficiently via their male siblings. This process would offer a benefit to sexual reproduction that may partly compensate for its costs, and therefore yields insight to the prevalence of sex in nature.