Animals can exhibit remarkable reproductive plasticity in response to their social surroundings, with profound fitness consequences. The study of such plasticity in females, particularly in same-sex interactions, has been severely neglected. Here we measured the impact of variation in the pre-mating social environment on reproductive success in females and tested the underlying mechanisms involved. We used the Drosophila melanogaster model system to test the effect of varying female group size prior to mating and deployed physical and genetic methods to manipulate the perception of different social cues and sensory pathways. We found that socially isolated females were significantly more likely to retain unfertilised eggs before mating, but to show the opposite pattern and lay significantly more fertilised eggs in the 24h after mating, in comparison to grouped females. More than 48h of exposure to other females was necessary for this socially-induced plasticity to be expressed. Neither olfactory nor visual cues were involved in mediating these responses. Instead, we found that females detected other females through direct contact with the deposits they leave behind, even in the absence of eggs. The results demonstrate that females show striking reproductive plasticity in response to their social surroundings and that the nature of their plastic reproductive responses, and the cues they use, differ markedly from those of males. The results emphasise the stark contrasts in how each sex realises reproductive success.

Background Animals can exhibit remarkable reproductive plasticity in response  to their social surroundings, with profound fitness consequences. The presence of same-sex conspecifics can signal current or future expected competition for resources or mates. Plastic responses to elevated sexual competition caused by exposure to same-sex individuals have been well-studied in males. However, much less is known about such plastic responses in females, whether this represents sexual or resource competition, or if it leads to changes in investment in mating behaviour and/or reproduction. Here, we used Drosophila melanogaster to measure the impact of experimentally varying female exposure to other females prior to mating on fecundity before and after mating. We then deployed physical and genetic methods to manipulate the perception of different social cues and sensory pathways and reveal the potential mechanisms involved. Results The results showed that females maintained in social isolation prior to mating were significantly more likely to retain unfertilised eggs before mating, but to show the opposite and lay significantly more fertilised eggs in the 24h after mating. More than 48h of exposure to other females was necessary for this social memory response to be expressed. Neither olfactory nor visual cues were involved in mediating fecundity plasticity—instead, the relevant cues were perceived through direct contact with the non-egg deposits left behind by other females. Conclusions The results demonstrate that females show reproductive plasticity in response to their social surroundings and can carry this memory of their social experience forward through mating. Comparisons of our results with previous work show that the nature of female plastic reproductive responses and the cues they use differ markedly from those of males. The results emphasise the deep divergence in how each sex realises its reproductive success.

Reproductive Interference occurs when interactions between individuals from different species disrupt reproductive processes, resulting in a fitness cost to one or both parties involved. It is typically observed between individuals of closely related species, often upon secondary contact. In both vertebrates and invertebrates, Reproductive Interference is frequently referred to as ‘Satyrisation’. It can manifest in various ways, ranging from blocking or reducing the efficacy of mating signals, through to negative effects of heterospecific copulations and the production of sterile or infertile hybrid offspring. The negative fitness effects of Satyrisation in reciprocal matings between species are often asymmetric and it is this aspect, which is most relevant to, and can offer utility in, pest management. In this review, we focus on Satyrisation and outline the mechanisms through which it can operate. We illustrate this by using test cases, and we consider the underlying reasons why the reproductive interactions that comprise Satyrisation occur. We synthesise the key factors affecting the expression of Satyrisation and explore how they have potential utility in developing new routes for the management and control of harmful insects. We consider how Satyrisation might interact with other control mechanisms, and conclude by outlining a framework for its use in control, highlighting some of the important next steps.

The satyr of Greek mythology was half‐man, half‐goat, with an animal persona signifying immoderate sexual appetites. In biology, satyrization is the disruption of reproduction in matings between closely related species. Interestingly, its effects are often reciprocally asymmetric, manifesting more strongly in one direction of heterospecific mating than the other. Heterospecific matings are well known to result in female fitness costs due to the production of sterile or inviable hybrid offspring and can also occur due to reduced female sexual receptivity, lowering the likelihood of any subsequent conspecific matings. Here we investigated the costs and mechanisms of satyrization in the Drosophila melanogaster species subgroup of fruitflies. The results showed that D. simulans females experienced higher fitness costs from a loss of remating opportunities due to significantly reduced post‐mating sexual receptivity than did D. melanogaster females, as a result of reciprocal heterospecific matings. Reciprocal tests of the effects of male reproductive accessory gland protein (Acp) injections on female receptivity in pairwise comparisons between D. melanogaster and five other species within the melanogaster species subgroup revealed significant post‐mating receptivity asymmetries. This was due to variation in the effects of heterospecific Acps within species with which D. melanogaster can mate, and significant but nonasymmetric Acp effects in species with which it cannot. We conclude that asymmetric satyrization due to post‐mating effects of Acps may be common among diverging and hybridising species. The findings are of interest in understanding the evolution of reproductive isolation and species divergence.