The genetic basis and fitness consequences of sperm midpiece size in deer mice.

Heidi S Fisher,Emily Jacobs-Palmer,Hopi E Hoekstra,Jean-Marc Lassance

doi:10.1038/ncomms13652

Abstract

An extensive array of reproductive traits varies among species, yet the genetic mechanisms that enable divergence, often over short evolutionary timescales, remain elusive. Here we examine two sister-species of Peromyscus mice with divergent mating systems. We find that the promiscuous species produces sperm with longer midpiece than the monogamous species, and midpiece size correlates positively with competitive ability and swimming performance. Using forward genetics, we identify a gene associated with midpiece length: Prkar1a, which encodes the R1α regulatory subunit of PKA. R1α localizes to midpiece in Peromyscus and is differentially expressed in mature sperm of the two species yet is similarly abundant in the testis. We also show that genetic variation at this locus accurately predicts male reproductive success. Our findings suggest that rapid evolution of reproductive traits can occur through cell type-specific changes to ubiquitously expressed genes and have an important effect on fitness.

Highlights

An extensive array of reproductive traits varies among species, yet the genetic mechanisms that enable divergence, often over short evolutionary timescales, remain elusive
We found that sperm head size does not differ between these species (Fig. 1b,c), but P. maniculatus sperm have longer flagella than P. polionotus (Fig. 1d; t-test: P 1⁄4 8 Â 10 À 11, df 1⁄4 9, n 1⁄4 10 sperm/ male)
We identified a single chromosomal region significantly associated with midpiece length variation on linkage group 4 (LG4; Fig. 3; on the basis of logarithm of odds [Logarithm of Odds (LOD)], significance determined by a genome-wide permutation test with a 1⁄4 0.01)

Summary

Introduction

An extensive array of reproductive traits varies among species, yet the genetic mechanisms that enable divergence, often over short evolutionary timescales, remain elusive. Because most genes expressed in reproductive organs (for example, testis) are expressed elsewhere in the body[5,6], genetic changes that result in reproductive trait modification can potentially lead to negative pleiotropic consequences in either the opposite sex or in other tissues Despite these constraints, reproductive phenotypes show striking and often rapid divergence, and can promote speciation[7]. We examine the relationship between sperm midpiece length, swimming performance and reproductive success in P. maniculatus, P. polionotus, and a hybrid population. We identify a single gene of large effect that regulates the phenotypic difference in sperm midpiece length between the two focal species, and show how allelic variation at this locus influences sperm swimming velocity and male fertility

Methods

Results

Conclusion