Differential selection between the sexes and the evolution of recombination in diploid and haplodiploid species

Abstract

The exchange of genetic material between homologous chromosomes during meiosis (i.e., genetic recombination) is a fundamental process that generates genetic diversity and influences evolutionary dynamics. Important variation in recombination rates can be observed at different phylogenetic scales with several broad patterns. In particular, eusocial hymenopterans (which are almost invariably haplodiploid) display some of the highest recombination rates among all eukaryotes. Among diploid species, females often have a higher recombination rate than males. The explanations for these phenomena are still unclear. We explore to what extent differences in selection between males and females may explain these patterns. To test these hypotheses, we use analytical modelling and individual-based, multilocus simulations in which fitness variation is caused by recurrent deleterious mutations occurring along a linear chromosome and in which the genetic map length of the chromosome (number of crossovers at meiosis) can evolve. We examined the effects of stronger selection against and stronger negative epistasis between deleterious mutations in males, which could possibly be caused by sexual selection among males, on the evolution of recombination rates. Our results show that negative epistasis among deleterious mutations does result in higher recombination rates in haplodiploids than in diploids. Negative epistasis restricted to males also generates a sexual dimorphism in recombination rates (aka heterochiasmy) in diploids consistent with the empirical pattern of higher recombination in females than males. In haplodiploids, higher recombination rates are favoured in meioses that produce parthenogenetic eggs (that will develop into males) than in meioses that produce fertilised eggs (that will develop into females). These results show that negative epistasis and sex-based differences in selection may explain the elevated recombination rates of eusocial hymenopterans and the patterns of heterochiasmy in diploid species.