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

Genes involved in reproduction often evolve rapidly at the sequence level 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 reproductive tract gene expression in natural populations, we captured adult males from monogamous Peromyscus californicus and polygynandrous P. boylii and P. maniculatus. We generated RNAseq libraries, quantified gene expression in the testis, seminal vesicle, epididymis, and liver, and identified 3627 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 behaviour in the seminal vesicles, where 89% of differentially expressed genes were MS-DEGs, including the key seminal fluid proteins Svs2 and Pate4. We also used published rodent genomes to test for positive and relaxed selection on Peromyscus-expressed genes. Though we did not observe more overlap than expected by chance between MS-DEGs and positively selected genes, 203 MS-DEGs showed evidence of positive selection. Fourteen reproductive genes were under tree-wide positive selection but 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 behaviour suggest that male mice may respond to sexual selection intensity by altering aspects of sperm motility, sperm-egg binding and copulatory plug formation.