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Female Drosophila melanogaster with environmentally or genetically elevated rates of mating die younger than controls. This cost of mating is not attributable to receipt of sperm. We demonstrate here that seminal fluid products from the main cells of the male accessory gland are responsible for the cost of mating in females, and that increasing exposure to these products increases female death rate. Main-cell products are also involved in elevating the rate of female egg-laying, in reducing female receptivity to further matings and in removing or destroying sperm of previous mates. The cost of mating to females may therefore represent a side-effect of evolutionary conflict between males.

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Mating induces profound changes in female insect behavior and physiology. In Drosophila melanogaster, mating causes a reduction in sexual receptivity and an elevation in egg production for at least 5 days. Injection of the seminal fluid sex peptide (SP) induces both responses in virgin females, but only for 1-2 days. The role of SP in eliciting the responses to mating remains to be elucidated. Functional redundancy between seminal fluid components may occur. In addition, mating with spermless males results in brief (1-to 2-day) post-mating responses, indicating either that there is a ''sperm effect'' or that sperm act as carriers for SP or other seminal fluid components. Here we used RNA interference to suppress SP expression, to determine whether SP is required to elicit full post-mating responses, the magnitude of responses due to other seminal fluid components, and whether SP accounts for the ''sperm effect.'' Receptivity was higher and egg production lower in females mated to SP knock-down males than in controls. Comparison with virgins showed that the responses were brief. SP is therefore required for normal magnitude and persistence of postmating responses. Sperm transfer and use were normal in mates of SP knock-down males, yet their post-mating responses were briefer than after normal matings, and similar to those reported in mates of spermless son-of-tudor males. The prolonged ''sperm effect'' on female receptivity and egg production is therefore entirely attributable to SP, but sperm are necessary for its occurrence.

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.

The seminal fluid of male Drosophila contains a cocktail of proteins that have striking effects on male and female fitness. In D. melanogaster, seminal fluid proteins affect female receptivity, ovulation, oogenesis, sperm storage, sperm competition and mating plug formation. In addition, the seminal fluid contains antibacterial peptides and protease inhibitors. Some seminal fluid-encoding genes also show high rates of evolutionary change, exhibiting both significant between-species divergence and within-species polymorphism. Seminal fluid protein genes are expressed only in males, begging the question of how and why the reproductive processes of females are influenced by males. In this review I address these issues by bringing together evidence for the function, evolution, diversification, and maintenance of variation in, seminal fluid-mediated traits.