Sexual antagonism, mating systems, and recombination suppression on sex chromosomes

Abstract

The suppression of recombination between sex chromosomes is a widespread feature of genetic sex determination systems. Competing explanations for this evolution fall into two broad categories: recombination arrest driven by the capture of sexually antagonistic variation versus arrest driven without sex-specific selection. Using population-genetic models, we compare the substitution rates of full recombination suppressors (such as inversions) driven by sexually antagonistic selection to those expected under neutrality. We consider both XY and ZW systems, mating ecologies ranging from random mating to polygyny with high male reproductive variance, suppressors arising on heterogametic (Y or W) versus homogametic (X or Z) chromosomes, and the effects of deleterious alleles segregating at other loci on the chromosome. We find that even very weak sexual antagonism is sufficient to expedite suppressor substitution by orders of magnitude relative to neutrality. This acceleration is robust to the presence of deleterious variation, although high variance in male reproductive success can diminish substitution rates of Y-linked suppressors in XY systems. By contrast, in ZW systems, elevated male reproductive variance tends to favour faster recombination arrest via W-linked suppressors, leading to higher overall rates of suppression than in comparable XY systems. Despite stronger selection on Y/W-linked suppressors, recombination arrest driven by sexual antagonism is often expected to arise from homogametic (X/Z-linked) suppressors, because their mutational input is higher and they can experience weaker drift. Together, these results yield testable predictions for the genomic distribution of sex-chromosome inversions across taxa differing in mating system and sex-determination system.