Mating partners often have conflicting interests when copulating. One of the major agents affecting female mating partners is seminal fluid, transferred along with sperm. The role of seminal fluid proteins (SFPs) in reproductive success is well studied in separate-sexed animals but is much less so in simultaneous hermaphrodites. The latter potentially have a unique target to exploit for the sperm donor's own benefit: the male function of their mating partners. Here we show that, in the great pond snail Lymnaea stagnalis, receipt of specific SFPs reduces both sperm transfer and paternity success in a subsequent insemination event. Lowering investment in the mating partner's male function constitutes a novel role for SFPs. This demonstrates for the first time that hermaphrodites alter their mates' male as well as female reproductive output. Although it remains to be tested whether this represents mate manipulation or an adaptive response of recipients, our findings identify male investment as a new target for postcopulatory sexual selection.
Lay summaryQuite a few animals are male and female at the same time, so they can choose to mate either as male or female on copulation. The decision to perform either sex role was known to be highly flexible depending on various, but often confounding, factors. For the pond snail, we report that young and small snails tend to mate as males first, though old and large snails do not seem to be better females.
An individual optimizes its reproductive success by adopting a particular reproductive strategy. Studying the details of a reproductive strategy leads to an understanding of how sexual selection acts, as the former is the process via which the individual reproduces successfully. Hermaphroditic gastropods display a bewildering diversity of reproductive strategies, which may be due to their mode of gender expression, when compared with well-studied separate-sexed species. Extensive theoretical, observational, and experimental research has been conducted on this topic. However, despite our knowledge about the reproductive system of hermaphroditic gastropods, we still need to fill the gap between pre- and post-copulatory processes and reproductive success. Here, we review and propose conceptual and empirical approaches aimed at understanding reproductive strategies of hermaphroditic gastropods. In sum, our suggestions are (i) to focus on sex-biased traits, (ii) to take biologically reliable measurements at both the pre- and post-copulatory level that relate to reproductive success, and (iii) to examine the fitness consequences of biased sex allocation.
Development is left–right reversed between dextral and sinistral morphs of snails. In sympatry, they share the same gene pool, including polygenes for shell shape. Nevertheless, their shell shapes are not the mirror images of each other. This triggered a debate between hypotheses that argue either for a developmental constraint or for zygotic pleiotropic effects of the polarity gene. We found that dextrals can be wider or narrower than sinistrals depending on the population, contrary to the prediction of invariable deviation under a developmental constraint. If the pleiotropy is solely responsible instead, the mean shape of each morph should change, depending on the frequency of polarity genotype. Our simulations of this mean shape change under zygotic pleiotropy, however, show that the direction of interchiral difference remains the same regardless of genotype frequency. Our results suggest the presence of genetic variation among populations that changes the maternal or zygotic pleiotropic effect of the polarity gene.
Seminal fluid proteins (SFPs, also referred to as accessory gland proteins or ACPs) contained in the ejaculate are transferred together with sperm to mating partners. Laboratory studies have examined within-population variation of SFPs at sequence, expression and functional levels, and established that these proteins exhibit a wide range of functions, such as inducing ovulation or defending mating
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