Reproductive plasticity in both sexes interacts to determine mating behaviour and fecundity

Abstract

Organisms alter their phenotype in response to variation in their environment by expressing phenotypic plasticity. Both sexes exhibit such plasticity in response to contrasting environmental and social cues, and this can reflect the influence of sexual conflict. However, theory predicts that plasticity expressed by both sexes may either maximise the sex-specific fitness of both, or of one sex at the expense of the other. Hence empirical tests of the predictions are sorely needed. Here we conducted novel tests of the fitness effects of interacting reproductive plasticity in Drosophila melanogaster. First, prior to mating, males were kept alone, or with same sex rivals, and females were kept alone, in same sex, or mixed sex groups. Second, we conducted matings between individuals from all these social treatments under ‘choice’ and ‘no choice’ scenarios. The results showed that males and females can both plastically respond to these socio-sexual environments to influence the expression of mating duration, mating latency, and fecundity. These plastic responses interacted significantly to determine mating latency and fecundity. Effects on mating latency were also observed under both choice and no-choice conditions, but in opposing directions. Variation in the outcome of interacting plasticity pivoted around the outcomes observed with focal females that had been maintained in same-sex environments prior to mating. However, not all fitness-related traits examined responded in the same way. Mating duration was determined largely by the social environment of the male. Our results show that the expression of some, but not all fitness-related reproductive traits can be determined by the outcome of interacting behavioural plasticity expressed by both sexes. This highlights the need for new predictive theory informed by these empirically-derived parameters. Overall, we conclude that variation in the expression of shared traits due to interacting plasticity represents an important and novel facet of sexual interactions. Impact Summary Animals and plants are able to respond to variation in their environment by expressing phenotypic plasticity. In sexual organisms, both males and females can exhibit such plasticity but the cues they respond to and the fitness consequences of these actions may be different between the sexes, and even conflicting. For example, males may respond to the presence of competitors by altering their mating behaviour or ejaculate transfer to increase their own, but not necessarily their mate’s reproductive output. However, females may also express phenotypic plasticity in response to their social and sexual environment to maximise their own fitness. Theory suggests that plasticity expressed by both sexes may either maximise the sex-specific fitness of both, or of one sex at the expense of the other. So far, little experimental work has been conducted to explore such interacting plasticity. Here we conducted novel tests of the fitness effects of interacting plasticity in the fruit fly Drosophila melanogaster. In doing so, we provide novel experimental evidence for interacting behavioural plasticity. We show that males and females can plastically respond to their socio-sexual environment to influence the expression of mating duration, mating latency, and fecundity. These plastic responses, while induced to increase the fitness interests of each sex, interact in the case of mating latency and fecundity and may reflect the outcome of sexual conflict. Our findings suggest that studies of reproductive behaviour should carefully consider the socio-sexual environment of both males and females and highlight the need for new predictive theory informed by empirically-derived parameters. Overall, we show that interacting plasticity between sexes represents an important and novel facet of sexual interactions.