Sperm competition risk drives plasticity in seminal fluid composition

Abstract

BackgroundEjaculates contain a diverse mixture of sperm and seminal fluid proteins, the combination of which is crucial to male reproductive success under competitive conditions. Males should therefore tailor the production of different ejaculate components according to their social environment, with particular sensitivity to cues of sperm competition risk (i.e. how likely it is that females will mate promiscuously). Here we test this hypothesis using an established vertebrate model system, the house mouse (Mus musculus domesticus), combining experimental data with a quantitative proteomics analysis of seminal fluid composition. Our study tests for the first time how both sperm and seminal fluid components of the ejaculate are tailored to the social environment.ResultsOur quantitative proteomics analysis reveals that the relative production of different proteins found in seminal fluid – i.e. seminal fluid proteome composition – differs significantly according to cues of sperm competition risk. Using a conservative analytical approach to identify differential expression of individual seminal fluid components, at least seven of 31 secreted seminal fluid proteins examined showed consistent differences in relative abundance under high versus low sperm competition conditions. Notably three important proteins with potential roles in sperm competition – SVS 6, SVS 5 and CEACAM 10 – were more abundant in the high competition treatment groups. Total investment in both sperm and seminal fluid production also increased with cues of heightened sperm competition risk in the social environment. By contrast, relative investment in different ejaculate components was unaffected by cues of mating opportunities.ConclusionsOur study reveals significant plasticity in different ejaculate components, with the production of both sperm and non-sperm fractions of the ejaculate strongly influenced by the social environment. Sperm competition risk is thus shown to be a key factor in male ejaculate production decisions, including driving plasticity in seminal fluid composition.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0197-2) contains supplementary material, which is available to authorized users.

Exposure to male-dominated environments during development influences sperm sex ratios at sexual maturity

“…Certainly, elevated testosterone levels is likely to be the underlying mechanism responsible for the development of enhanced body size, testes size, and AGD (Zielinski and Vandenbergh ), which, among mammals, are commonly observed responses to increased competition within the postmaternal environment (Ramm et al. ; André et al. ; Firman et al.…”

Sexual selection, phenotypic plasticity and female reproductive output

“…In other cases, the plastic response is not in the predicted direction. For example, there were no consistent effects of perceived future mating opportunities on investment into either pre or post-copulatory sexual traits by guppies [121]; nor did male mice adjust their ejaculates to the number of potential mating opportunities, although they did so in response to the perceived risk of sperm competition [122]. These anomalies might arise because the marginal benefits of allocating resources to different sexually selected traits depend on the level of mating and fertilization competition [114].…”

The molecular basis and reproductive function(s) of copulatory plugs

“…Given the cost of ejaculation, selection may favor males that avoid mating in second place (Ramm and Stockley, ). The very existence of male mate choice, rather than indiscriminant mating (Drickamer et al, ; Gowaty et al, ; Edward and Chapman, ), and evidence that males adjust their ejaculates when presented with sub‐optimal mating opportunities (Pizzari et al, ; Delbarco‐Trillo and Ferkin, ; Ramm and Stockley, ; Lüpold et al, ; DelBarco‐Trillo, ; Ramm et al, ) together imply that ejaculates are physiologically expensive and are conserved whenever possible (Parker, ; Parker and Pizzari, ). Indeed, direct calorimetric study revealed that a single copulatory plug in garter snakes might represent 5–18% of an animal's daily energy budget (Friesen et al, ).…”