Sex-specific evolutionary programs shape recombination rate evolution in house mice

Recombination rates vary across species, populations, and sexes. House mice (Mus musculus) present a particularly extreme example. Prior studies have established large differences in global recombination rates between M. musculus subspecies and inbred strains, with males exhibiting more extensive variation than females. The observation of sex-limited variation has prompted the hypothesis that male and female recombination rates may evolve by distinct evolutionary mechanisms in M. musculus. Here, we formally evaluate this hypothesis in a phylogenetic framework. We combine cytogenetic estimates of genomic crossover counts with published data to compile a large dataset of sex-specific crossover rate estimates totaling >6,000 single meiotic cells from 31 genetically diverse inbred mouse strains representing five Mus species and four M. musculus subspecies. We show that the phylogenetic distribution of male recombination rates is well predicted by the underlying Mus phylogeny (phylogenetic heritability, HP2 = 0.82), contrasting with the weaker phylogenetic signal observed in females (HP2 = 0.24). M. m. musculus males exhibit a marked increase in recombination rate compared to males from other M. musculus subspecies, prompting us to test explicit models of lineage-specific evolution. We uncover evidence for an adaptive increase in male recombination rate along the M. m. musculus subspecies lineage but find no support for a parallel increase in females. Taken together, our findings confirm the hypothesis that recombination rate evolution in house mice is governed by distinct sex-specific evolutionary regimes and motivate future efforts to ascertain the sex-specific selective pressures and sex-specific genetic architectures that underlie these observations.