Divergence of seminal fluid gene expression and function among natural snail populations.

Alice Thornton Smith,Léa Daupagne,Yumi Nakadera,Marie‐Agnès Coutellec,Joris M Koene,Steven A Ramm

doi:10.1111/jeb.13683

Abstract

Seminal fluid proteins (SFPs) can trigger drastic changes in mating partners, mediating post-mating sexual selection and associated sexual conflict. Also, cross-species comparisons have demonstrated that SFPs evolve rapidly and hint that post-mating sexual selection drives their rapid evolution. In principle, this pattern should be detectable within species as rapid among-population divergence in SFP expression and function. However, given the multiple other factors that could vary among populations, isolating divergence in SFP-mediated effects is not straightforward. Here, we attempted to address this gap by combining the power of a common garden design with functional assays involving artificial injection of SFPs in the simultaneously hermaphroditic freshwater snail, Lymnaea stagnalis. We detected among-population divergence in SFP gene expression, suggesting that seminal fluid composition differs among four populations collected in Western Europe. Furthermore, by artificially injecting seminal fluid extracted from these field-derived snails into standardized mating partners, we also detected among-population divergence in the strength of post-mating effects induced by seminal fluid. Both egg production and subsequent sperm transfer of partners differed depending on the population origin of seminal fluid, with the response in egg production seemingly closely corresponding to among-population divergence in SFP gene expression. Our results thus lend strong intraspecific support to the notion that SFP expression and function evolve rapidly, and confirm L. stagnalis as an amenable system for studying processes driving SFP evolution.

Highlights

Seminal fluid proteins (SFPs, referred to as accessory gland proteins or ACPs) contained in the ejaculate are transferred together with sperm to mating partners
We focused on measuring the egg production and sperm transfer of standardized focal snails that had each been artificially injected with prostate gland extracts from one of the field-derived families
We found clear evidence that SFP gene expression differs among natural populations of L. stagnalis and demonstrate using an artificial injection that this likely has functional consequences for egg production and subsequent sperm transfer by SFP recipients

Summary

| INTRODUCTION

Seminal fluid proteins (SFPs, referred to as accessory gland proteins or ACPs) contained in the ejaculate are transferred together with sperm to mating partners. We aim here to expand the scope of studying intraspecific variation in SFPs, using the simultaneously hermaphroditic great pond snail, Lymnaea stagnalis, by utilizing the following advantages, especially the known functions of their SFPs and an established bioassay This species is abundant, widespread, and populations are genetically well-structured (Bouétard, Côte, Besnard, Collinet, & Coutellec, 2014; Kopp, Wolff, & Jokela, 2012; Nakadera, Mariën, Van Straalen, & Koene, 2017; Puurtinen, Hytönen, et al, 2004; Puurtinen, Knott, Suonpää, Ooik, & Kaitala, 2004). We have an established SFP bioassay based on intravaginally injecting seminal fluid in L. stagnalis (Koene, Hoffer, & Brouwer, 2009; Koene et al, 2010; Nakadera et al, 2014) This species provides an excellent opportunity to examine the functional consequences of intraspecific variation in SFP expression in controlled laboratory experiments. Through a series of gene expression and follow-up functional assays of SFPs, we first tested whether seminal fluid expression differs consistently among populations and whether this leads to corresponding variation in partner responses to SFP receipt

| MATERIALS AND METHODS

Findings

| DISCUSSION