Deleterious mutations can contribute to the evolution of recombination suppression between sex chromosomes

Abstract

Many organisms have sex chromosomes with large non-recombining regions that expand in a stepwise manner, although the underlying reasons remain poorly understood. Recently, we proposed that recombination suppression may evolve in sex chromosomes simply because of the presence of recessive deleterious mutations within genomes. Specifically, we demonstrated that chromosomal inversions suppressing recombination and carrying by chance fewer deleterious mutations than average have a selective advantage. In addition, we showed that the permanent heterozygosity of Y-like sex chromosomes facilitates the fixation of these less-loaded inversions by a sheltering effect, i.e., by preventing the expression of recessive deleterious mutations in a homozygous state when they increase in frequency. In contrast, similar less-loaded inversions in autosomes suffer from a disadvantage in the homozygous state as their frequency increases, preventing their fixation. However, the methodology and significance of our previous study have been questioned. Here, we present new analyses that further reinforce our original claims, demonstrating that the lower-load advantage and the sheltering effect can explain the fixation of inversions on sex chromosomes over a broad range of parameter values. We show that these mechanisms promote the fixation of inversions on Y-like chromosomes at rates exceeding those expected under drift alone. We used, as a control, autosomes with a similar population size as the Y chromosome, which, we argue, provides the appropriate neutral control for the sheltering effect. We also address criticisms regarding our focus on inversions surviving the first 20 generations in a figure of our previous study, and show that these criticisms stemmed from a misunderstanding of what this figure was intended to illustrate. Including all inversions, even those that went extinct within 20 generations, does not alter our conclusions. Overall, the present study offers new support for our theory based on the combination of lower-load advantage and sheltering effect, and addresses the questions about its significance and range of applicability.