Sexual antagonism drives the displacement of polymorphism across gene regulatory cascades

Abstract

Males and females have different reproductive roles and are often subject to contrasting selection pressures. This sexual antagonism can lead, at a given locus, to different alleles being favoured in each sex and, consequently, to genetic variation being maintained in a population. Although the presence of antagonistic polymorphisms has been documented across a range of species, their evolutionary dynamics remain poorly understood. Here we study antagonistic selection on gene expression, which is fundamental to sexual dimorphism, via the evolution of regulatory binding sites. We show that for sites longer than 1 nucleotide, polymorphism is maintained only when intermediate expression levels are deleterious to both sexes. We then show that, in a regulatory cascade, polymorphism tends to become displaced over evolutionary time from the target of antagonistic selection to upstream regulators. Our results have consequences for understanding the evolution of sexual dimorphism, and provide specific empirical predictions for the regulatory architecture of genes under antagonistic selection