Abstract

BackgroundMale seminal fluid proteins (SFPs), transferred to females during mating, are important reproductive proteins that have multifarious effects on female reproductive physiology and that often show remarkably rapid and divergent evolution. Inferences regarding natural selection on SFPs are based primarily on interspecific comparative studies, and our understanding of natural within-species variation in SFPs and whether this relates to reproductive phenotypes is very limited. Here, we introduce an empirical strategy to study intraspecific variation in and selection upon the seminal fluid proteome. We then apply this in a study of 15 distinct populations of the seed beetle Callosobruchus maculatus.ResultsPhenotypic assays of these populations showed significant differences in reproductive phenotypes (male success in sperm competition and male ability to stimulate female fecundity). A quantitative proteomic study of replicated samples of male accessory glands revealed a large number of potential SFPs, of which ≥127 were found to be transferred to females at mating. Moreover, population divergence in relative SFP abundance across populations was large and remarkably multidimensional. Most importantly, variation in male SFP abundance across populations was associated with male sperm competition success and male ability to stimulate female egg production.ConclusionsOur study provides the first direct evidence for postmating sexual selection on standing intraspecific variation in SFP abundance and the pattern of divergence across populations in the seminal fluid proteome match the pattern predicted by the postmating sexual selection paradigm for SFP evolution. Our findings provide novel support for the hypothesis that sexual selection on SFPs is an important engine of incipient speciation.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0547-2) contains supplementary material, which is available to authorized users.

Highlights

  • Male seminal fluid proteins (SFPs), transferred to females during mating, are important reproductive proteins that have multifarious effects on female reproductive physiology and that often show remarkably rapid and divergent evolution

  • Proteomics assays Our analysis showed that the male accessory gland proteome of C. maculatus is composed of at least 683 distinct Acps (Fig. 1)

  • Because each PC captures a unique aspect of multivariate variation, it shows that significant differences across populations in the accessory gland proteome occur along many distinct multivariate dimensions

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Summary

Introduction

Male seminal fluid proteins (SFPs), transferred to females during mating, are important reproductive proteins that have multifarious effects on female reproductive physiology and that often show remarkably rapid and divergent evolution. We introduce an empirical strategy to study intraspecific variation in and selection upon the seminal fluid proteome. We apply this in a study of 15 distinct populations of the seed beetle Callosobruchus maculatus. In virtually all animals with internal fertilization, male accessory reproductive glands produce a complex cocktail of seminal fluid proteins (SFPs) that are transferred to females during mating. These reproductive proteins have attracted much research interest during the last two decades for at least four related reasons.

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