Evolution and co-evolution of the suck behaviour, a postcopulatory female resistance trait that manipulates received ejaculate

Abstract

Sexual conflicts over the post-mating fate of received ejaculate can favour traits in one sex that are costly to the other. Reciprocally mating hermaphrodites face unique challenges as they mate simultaneously in both the male and female role, potentially leading to receipt of unwanted ejaculate. Reciprocal mating can then give rise to postcopulatory female resistance traits that allow manipulation of received ejaculate. A putative example is the suck behaviour, observed in the flatworm genus Macrostomum. It involves the sperm recipient placing its pharynx over its own female genital opening and appearing to suck, likely removing received ejaculate after mating. The genus also contains hypodermically-inseminating species that presumably exhibit unilateral mating and have not been observed to suck. Here, we examine the evolution of the suck behaviour in Macrostomum, aiming to document the mating behaviour in 64 species. First, we provide videographic evidence that ejaculate is indeed removed during the suck behaviour in a reciprocally mating species, Macrostomum hamatum. Next, we show evolutionary positive correlations between the presence, duration and frequency of reciprocal mating behaviour and the suck behaviour, providing clear evidence that the suck behaviour co-evolves with reciprocal mating behaviour. Finally, we show an association between reproductive behaviour and reproductive morphology, suggesting that reproductive morphology can be used for inferring the behavioural mating strategy of a species. Together our study demonstrates sexual antagonistic coevolution leading to the evolution of a postcopulatory behavioural trait that functions as a female counter-adaptation allowing individuals to gain control over received ejaculate in a hermaphroditic sexual system.