Chromosome-specific drift under stabilizing selection generates polygenic barriers to sex chromosome turnover

Abstract

Sex chromosome systems show frequent evolutionary transitions in some clades, but long-term stability in others. Previous explanations of this stasis rely on evolutionary dynamics peculiar to sex chromosomes, such as the accumulation of deleterious mutations on the sex-specific chromosome or sexually antagonistic mutations on either sex chromosome. Here, I show that stabilizing selection on quantitative traits promotes stability of sex chromosome systems. The reason is that stabilizing selection, while keeping the value of the trait near its optimum, allows individual chromosomes contributions to the trait to drift, and this chromosome-specific drift reduces the fitness of the novel sexual genotypes necessarily produced during sex chromosome turnover. Given the ubiquity of stabilizing selection on quantitative traits, chromosome-specific drift could play a pivotal role in preventing the turnover of sex chromosome systems across multiple stages of their evolution and can explain key patterns in the phylogenetic distribution of sex-determining systems.