Sexual selection drives the coevolution of male and female reproductive traits in Peromyscus mice

Abstract

When females mate with multiple partners within a single reproductive cycle, sperm from rival males may compete for fertilization of a limited number of ova, and females may bias the fertilization of their ova by particular sperm. Over evolutionary timescales, these two forms of selection shape both male and female reproductive physiology when females mate multiply, yet in monogamous systems, post‐copulatory sexual selection is weak or absent. Here, we examine how divergent mating strategies within a genus of closely related mice, Peromyscus, have shaped the evolution of reproductive traits. We show that in promiscuous species, males exhibit traits associated with increased sperm production and sperm swimming performance, and females exhibit traits that are predicted to limit sperm access to their ova including increased oviduct length and a larger cumulus cell mass surrounding the ova, compared to monogamous species. Importantly, we found that across species, oviduct length and cumulus cell density are significantly correlated with sperm velocity, but not sperm count or relative testes size, suggesting that these female traits may have coevolved with increased sperm quality rather than quantity. Taken together, our results highlight how male and female traits evolve in concert and respond to changes in the level of post‐copulatory sexual selection.

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

“…In monogamous P. californicus , male-male competition is reduced and postcopulatory sexual selection should be weak in comparison with polygynandrous P. maniculatus and P. boylii . A recent study showed that traits under postcopulatory sexual selection, such as sperm production efficiency and sperm swimming speed, are increased and show a stronger correlation with female defensiveness traits such as oviduct length in more polygynandrous Peromyscus (Weber and Fisher 2023). This suggests that the extent of both male-male competition and male-female sexual conflict varies with mating behavior.…”

“…Further, Adgrd1 is an MS-DEG with reduced expression in the P. californicus seminal vesicle and epididymis. Exploring female reproductive tract gene expression would address whether any 'male fertility' genes are expressed in the female reproductive tract or vice versa and would contribute to our understanding of female defense traits such as egg extracellular matrix and uterine fluid composition (Hook et al, 2022;Weber and Fisher 2023).…”

“…Mice in the genus Peromyscus provide an excellent opportunity to study the influence of mating system on both gene expression and protein sequence evolution for male reproductive genes. Polygynandry (loosely affiliative multimale -multifemale mating system) is the ancestral state in Peromyscus , and different species in this genus exhibit broad variation in mating ecology (Bedford and Hoekstra 2015;Meléndez-Rosa et al, 2019;Weber and Fisher 2023).…”