Antagonistic pleiotropy in species with separate sexes, and the maintenance of genetic variation in life‐history traits and fitness

Abstract

Antagonistic pleiotropy (AP)-where alleles of a gene increase some components of fitness at a cost to others-can generate balancing selection, and contribute to the maintenance of genetic variation in fitness traits, such as survival, fecundity, fertility, and mate competition. Previous theory suggests that AP is unlikely to maintain variation unless antagonistic selection is strong, or AP alleles exhibit pronounced differences in genetic dominance between the affected traits. We show that conditions for balancing selection under AP expand under the likely scenario that the strength of selection on each fitness component differs between the sexes. Our model also predicts that the vast majority of balanced polymorphisms have sexually antagonistic effects on total fitness, despite the absence of sexual antagonism for individual fitness components. We conclude that AP polymorphisms are less difficult to maintain than predicted by prior theory, even under our conservative assumption that selection on components of fitness is universally sexually concordant. We discuss implications for the maintenance of genetic variation, and for inferences of sexual antagonism that are based on sex-specific phenotypic selection estimates-many of which are based on single fitness components.

Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly

“…Differences between genotypes in size, development time, fertility and survival are stronger for males than for females. Within a range of realistic parameters, sex-specific effects, even without antagonism for each fitness components, results in sexual antagonism for total fitness, therefore strongly protecting polymorphism (23). Moreover, even without sexual antagonism in total fitness, our simulations suggest that sex-specific selection varying between components of fitness delays the fixation of alleles ( Fig S11).…”

“…In addition to environmental heterogeneity, polymorphism generated by antagonistic pleiotropy is predicted to be enhanced by different trade-off intensities for each sex (23). Sex-specific selection on different fitness components frequently occurs in nature since optimal age/size at maturity or the physiological state to achieve high fertility often differs between sexes (14,58,59).…”

“…Antagonistic pleiotropy has long been considered as a minor contributor to balancing selection because theoretical studies predicted it enables persistent polymorphism only for a limited range of parameters (20)(21)(22). Nevertheless, recent models suggest that the role of antagonistic pleiotropy has been underestimated (23)(24)(25)(26). Indeed, these new models show that several factors, realistic in natural populations, can promote polymorphism persistence.…”

“…when the level of dominance varies between fitness components (26,27)), sex-specific selection (i.e. selection strength on each fitness component differs between sexes (23)) and spatially and temporally varying selection (24,25).…”

Context-dependent genetic architecture of Drosophila life span

“…In addition, theories for the maintenance of quantitative genetic variation due to genotype-by-environment interaction (GEI) or genotype-by-sex interaction (GSI) also apply to life span. Alleles with environment-(or sex-)specific effects-or antagonistic effects in different environments or between the sexes-can be maintained at intermediate frequencies under some conditions [18][19][20][21][22][23].…”