Mating system variation and gene expression in the male reproductive tract of Peromyscus mice

Abstract

Genes involved in reproduction often evolve rapidly due to postcopulatory sexual selection (PCSS) driven by male-male competition and male-female sexual conflict, but the impact of PCSS on gene expression has been under-explored. Further, though multiple tissues contribute to male reproductive success, most studies have focused on the testes. To explore the influence of mating system variation on gene expression in the Peromyscus male reproductive tract, we generated RNAseq libraries and quantified gene expression in the testis, seminal vesicle, epididymis, and liver of wild-caught monogamous P. californicus and polygynandrous P. boylii and P. maniculatus males and tested for positive and relaxed selection on Peromyscus-expressed genes using published rodent genomes. We identified 3,627 mating-system associated differentially expressed genes (MS-DEGs), where expression shifted in the same direction in P. maniculatus and P. boylii relative to P. californicus. Gene expression variation was most strongly associated with mating behavior in the seminal vesicles, where 89% of differentially expressed genes were MS-DEGs, including two key seminal fluid proteins, Svs2 and Pate4. Though but most genes showing evidence of positive selection or differential expression did not overlap, 203 MS-DEGs showed evidence of positive selection. Additionally, fourteen reproductive genes were under tree-wide positive selection but showed evidence of convergent relaxed selection in P. californicus and Microtus ochrogaster, a distantly related monogamous species. Changes in transcript abundance and gene sequence evolution in association with mating behavior suggest that male mice may respond to variation in sexual selection by altering aspects of sperm motility, sperm-egg binding, and copulatory plug formation.