Abstract
The rate of meiotic recombination varies markedly between species and among individuals. Classical genetic experiments demonstrated a heritable component to population variation in recombination rate, and specific sequence variants that contribute to recombination rate differences between individuals have recently been identified. Despite these advances, the genetic basis of species divergence in recombination rate remains unexplored. Using a cytological assay that allows direct in situ imaging of recombination events in spermatocytes, we report a large (∼30%) difference in global recombination rate between males of two closely related house mouse subspecies (Mus musculus musculus and M. m. castaneus). To characterize the genetic basis of this recombination rate divergence, we generated an F2 panel of inter-subspecific hybrid males (n = 276) from an intercross between wild-derived inbred strains CAST/EiJ (M. m. castaneus) and PWD/PhJ (M. m. musculus). We uncover considerable heritable variation for recombination rate among males from this mapping population. Much of the F2 variance for recombination rate and a substantial portion of the difference in recombination rate between the parental strains is explained by eight moderate- to large-effect quantitative trait loci, including two transgressive loci on the X chromosome. In contrast to the rapid evolution observed in males, female CAST/EiJ and PWD/PhJ animals show minimal divergence in recombination rate (∼5%). The existence of loci on the X chromosome suggests a genetic mechanism to explain this male-biased evolution. Our results provide an initial map of the genetic changes underlying subspecies differences in genome-scale recombination rate and underscore the power of the house mouse system for understanding the evolution of this trait.
Highlights
Meiotic recombination fulfills dual roles in genetics and evolution
Recent studies have begun to unravel the genetic basis of recombination rate variation within populations, the genetic mechanisms of species divergence in recombination rate remain poorly characterized
We show that two closely related house mouse subspecies differ in their genomic recombination rates by,30%, providing an excellent model system for studying evolutionary divergence in this trait
Summary
Meiotic recombination fulfills dual roles in genetics and evolution. The improper patterning of recombination events across chromosomes can lead to aneuploidy, a significant risk factor for fetal loss and developmental disability in humans [4]. Recombination influences the evolutionary dynamics of populations by rearranging existing patterns of allelic variation to generate novel multi-locus genotypes. This genetic shuffling can increase the efficacy of natural selection by decoupling high fitness alleles from linked deleterious variation [5,6,7]. Recombination can facilitate the removal of deleterious variation from the gene pool [8,9]
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