Selection in males purges the mutation load on female fitness

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.