The Genetics of Sexually Selected Male Reproductive Traits in Mice (Mus and Peromyscus Species)

Abstract

Sexual selection is rampant in Nature, and has produced some of the most beautiful and bizarre traits on Earth. Because females are often promiscuous, sexual selection can continue even after mating, as the sperm of multiple males race to fertilize a limited number of eggs. Though post-copulatory sexual selection is ubiquitous and drives both rapid adaptation and divergence between lineages, we know little about the genetic basis of phenotypes subject to this force. To illuminate one of the important mechanisms by which evolution produces a remarkable diversity of traits, we must identify the genetic loci targeted by post-copulatory sexual selection. Here we determine the genes or genomic regions underlying particular male reproductive traits—sperm development and morphology, age to male sexual maturity, and segregation distortion—that were likely shaped by post-copulatory sexual selection in the ancestors of mice from the genera Peromyscus and Mus. We measure phenotype at the organismal and cellular levels, and then employ quantitative trait locus mapping, RNA sequencing, and bulk DNA sequencing to pinpoint loci influencing the aforementioned traits. We first identify a single locus of large effect controlling sperm midpiece length, a trait relevant to sperm competition success that differs between promiscuous and monogamous sister species of Peromyscus mice. We then show that regions of the genome underlying polymorphism in sperm morphology within species are entirely distinct from those determining divergence in the same traits between species. Next, we determine differences in age to male sexual maturity in closely related species with disparate mating systems, and characterize the role of cis-regulatory evolution in the timing of male reproductive development. Additionally, we develop a novel method to identify segregation distortion systems that may have been shaped by historical selection at multiple levels, but find none in hybrids of Mus musculus. Finally, we characterize the role of a non-coding RNA locus in male fertility, discovering that it mediates separation of spermatids from collective cytoplasm. In sum, we reveal links between particular genes or genomic regions and male reproductive phenotypes that may influence success in post-copulatory competition, thereby clarifying the mechanistic basis of evolution by sexual selection.