Person:

Jacobs-Palmer, Emily

Understanding the molecular basis of species formation is an important goal in evolutionary genetics, and Dobzhansky-Muller incompatibilities are thought to be a common source of postzygotic reproductive isolation between closely related lineages. However, the evolutionary forces that lead to the accumulation of such incompatibilities between diverging taxa are poorly understood. Segregation distorters are believed to be an important source of Dobzhansky-Muller incompatibilities between hybridizing species of Drosophila as well as hybridizing crop plants, but it remains unclear if these selfish genetic elements contribute to reproductive isolation in other taxa. Here, we collected viable sperm from first-generation hybrid male progeny of Mus musculus castaneus and M. m. domesticus, two subspecies of rodent in the earliest stages of speciation. We then genotyped millions of single nucleotide polymorphisms in these gamete pools and tested for a skew in the frequency of parental alleles across the genome. We show that segregation distorters are not measurable contributors to observed infertility in these hybrid males, despite sufficient statistical power to detect even weak segregation distortion with our novel method. Thus, reduced hybrid male fertility in crosses between these nascent species is attributable to other evolutionary forces.

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.

An extensive array of reproductive traits varies among species, yet the genetic mechanisms that enable divergence, often over short evolutionary timescales, remain elusive. Here we examine two sister-species of Peromyscus mice with divergent mating systems. We find that the promiscuous species produces sperm with longer midpiece than the monogamous species, and midpiece size correlates positively with competitive ability and swimming performance. Using forward genetics, we identify a gene associated with midpiece length: Prkar1a, which encodes the R1α regulatory subunit of PKA. R1α localizes to midpiece in Peromyscus and is differentially expressed in mature sperm of the two species yet is similarly abundant in the testis. We also show that genetic variation at this locus accurately predicts male reproductive success. Our findings suggest that rapid evolution of reproductive traits can occur through cell type-specific changes to ubiquitously expressed genes and have an important effect on fitness.