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.

Keywords: cryptic female choice; mammals; sexual conflicts; sexual selection; sperm competition.

FIGURE 1

Reproductive trait variation within and between Peromyscus species. Dots represents individual (a) male and (b) female trait values. Black bars indicate species mean. Monogamous species are shown as cool colours (teal, light‐blue and blue) and promiscuous species are shown as warm colours (orange, red and crimson). Species relatedness is shown below each x‐axis.

FIGURE 2

Statistically significantly intersexual correlations comparing reproductive traits across three monogamous species, P. californicus (P. cal), P. eremicus (P. ere) and P. polionotus (P. pol), and three promiscuous species, P. gossypinus (P. gos), P. leucopus (P. leu) and P. maniculatus (P. man). Monogamous species are shown as cool colours (teal, light‐blue and blue) and promiscuous species are shown as warm colours (orange, red and crimson).