Rodents of Unusual Sperm: Molecular and Phenotypic Evolution of Male Reproduction in Murine Rodents
Authors: Emily Kopania 1,2; Gregg Thomas 1,3; Carl Hutter 4; Sebastian Mortimer 1; Colin Callahan 1; William Breed 5; Nathan Clark 2; Jacob Esselstyn 4; Kevin Rowe 6; Jeffrey Good 1
Affiliations: 1) University of Montana; 2) University of Utah; 3) Harvard University; 4) Louisiana State University; 5) University of Adelaide; 6) Museums Victoria
Keywords: Comparative genomics & genome evolution
Male reproductive traits often evolve extremely rapidly, likely due to post-mating sexual selection. In parallel, genes expressed in reproductive tissues tend to diverge rapidly in protein-coding sequence, which is often attributed to positive selection. However, few studies have connected rapid phenotypic and molecular evolution for reproductive traits or directly tested the role of positive selection underlying divergence. Doing so requires species that vary in reproductive phenotypes, a well-resolved phylogeny, and information on genes expressed in reproductive tissues. Murine rodents provide an ideal system for studying reproductive evolution because they include the well-studied mouse and rat model systems and also represent a massive radiation (>10% of mammal species) with a remarkable diversity of reproductive phenotypes among species. In this study, we sequenced exomes from 209 murine species to infer a well-resolved phylogeny and modeled male reproductive trait evolution across this phylogeny for 96 species. We showed that relative testes mass, a proxy for sperm competition, was evolving independently of phylogeny. Most murine species have a hook on the sperm head, and our analyses showed that hook length and angle were correlated with relative testes mass, suggesting that these traits are likely co-evolving in response to sperm competition. We found that genes expressed in the seminal vesicles and during the later (post-meiotic) stages of spermatogenesis tended to be the most rapidly evolving among reproductive genes, and that this rapid evolution was due in part to more frequent positive directional selection. We also used these data to examine if some genes evolve rapidly in lineages with convergent reproductive traits such as large testes mass to directly connect the rapid molecular and phenotypic evolution of male reproduction. We tested if reproductive genes experienced episodic bursts of positive directional selection in lineages with elevated divergence in reproductive traits. Collectively, our results demonstrate that sperm competition and positive selection likely play a central role in the rapid phenotypic and molecular evolution of male reproductive traits in murine rodents, but the intensity of these forces and their importance in shaping evolutionary patterns is highly variable across traits, tissues, and species.