Conflicts between females and males over reproductive decisions are common . In Drosophila, as in many other organisms, there is often a conflict over how often to mate. The mating frequency that maximizes male reproductive success is higher than that which maximizes female reproductive success . In addition, frequent mating reduces female lifespan and reproductive success , a cost that is mediated by male ejaculate accessory gland proteins (Acps) . We demonstrate here that a single Acp, the sex peptide (SP or Acp70A), which decreases female receptivity and stimulates egg production in the first matings of virgin females , is a major contributor to Acp-mediated mating costs in females. Females continuously exposed to SP-deficient males (which produce no detectable SP ) had significantly higher fitness and higher lifetime reproductive success than control females. Hence, rather than benefiting both sexes, receipt of SP decreases female fitness, making SP the first identified gene that is likely to play a central role in sexual conflict.

Summary Post-copulatory sexual selection can select for sperm allocation strategies in males [1, 2] but males should also strategically allocate non-sperm components of the ejaculate [3, 4] such as seminal fluid proteins (Sfps). Sfps can influence the extent of post-copulatory sexual selection [5–7] but little is known of the causes or consequences of quantitative variation in Sfp production and transfer. Using Drosophila melanogaster, we demonstrate that Sfps are strategically allocated to females in response to the potential level of sperm competition. We also show that males who can produce and transfer larger quantities of specific Sfps have a significant competitive advantage. When males were exposed to a competitor male, matings were longer and more of two key Sfps, sex peptide [8] and ovulin [9], were transferred, indicating strategic allocation of Sfps. Males selected for large accessory glands (AGs, a major site of Sfp synthesis) produced and transferred significantly more sex peptide, but not more ovulin. Large AG males also had significantly increased competitive reproductive success. Our results show that quantitative variation in specific Sfps is likely to play an important role in post-copulatory sexual selection and that investment in Sfp production is essential for male fitness in a competitive environment.

Ejaculates are fundamental to fitness in sexually-reproducing animals: males gain all their direct fitness via the ejaculate and females require ejaculates to reproduce. Both sperm and non-sperm components of the ejaculate (including parasperm, seminal proteins, water and macromolecules) play vital roles in post-copulatory sexual selection and conflict, processes that can potentially drive rapid evolutionary change and reproductive isolation. Here, we assess the increasing evidence that considering ejaculate composition as a whole – and potential trade-offs among ejaculate components – has important consequences for predictions about male reproductive investment and female responses to ejaculates. We review current theory and empirical work, and detail how social and environmental effects on ejaculate composition have potentially far-reaching fitness consequences for both sexes.

Abstract. The interests of males and females over reproduction rarely coincide and conflicts between the sexes over mate choice, mating frequency, reproductive investment, and parental care are common in many taxa. In Drosophila melanogaster, the optimum mating frequency is higher for males than it is for females. Furthermore, females that mate at high frequencies suffer significant mating costs due to the actions of male seminal fluid proteins. Sexual conflict is predicted to lead to sexually antagonistic coevolution, in which selection for adaptations that benefit males but harm females is balanced by counterselection in females to minimize the extent of male-induced harm. We tested the prediction that elevated sexual conflict should select for increased female resistance to male-induced harm and vice versa. We manipulated the intensity of sexual conflict by experimentally altering adult sex ratio. We created replicated lines of D. melanogaster in which the adult sex ratio was male biased (high conflict lines), equal (intermediate conflict lines), or female biased (low conflict lines). As predicted, females from high sexual conflict lines lived significantly longer in the presence of males than did females from low conflict lines. Our conclusion that the evolutionary response in females was to the level of male-induced harm is supported by the finding that there were no female longevity differences in the absence of males. Differences between males in female harming ability were not detected. This suggests that the response in females was to differences between selection treatments in mating frequency, and not to differences in male harmfulness.

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