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.
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.
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.
Resolving the mechanisms that switch competition to cooperation is key to understand biological organization1. This is particularly relevant for intrasexual competition, which often leads to males harming females2. Recent theory proposes that kin selection may modulate female harm by relaxing competition among relatives3-5. We experimentally manipulated the relatedness of groups of male Drosophila melanogaster competing over females to demonstrate that, as expected, within group relatedness inhibits male competition and female harm. Females exposed to three brothers unrelated to the female had higher lifetime reproductive success and slower reproductive ageing compared to females exposed to triplets of males unrelated to each other. Triplets of brothers also fought less with each other, courted females less intensively and lived longer than triplets of unrelated males. However, associations among brothers may be vulnerable to invasion by minorities of unrelated males: when two brothers were matched with an unrelated male, the latter sired on average twice as many offspring as either brother. These results demonstrate that relatedness can profoundly affect fitness through its modulation of intrasexual competition, as flies plastically adjust sexual behaviour in a way consistent with kin selection theory.We first tested the effect of relatedness of males within a group on female fitness, by quantifying different aspects of fitness and life-history (experiment 1) in females exposed to male triplets. Males were unrelated to the female and either full-sib brothers of each other (AAA) or unrelated to each other (ABC), and were replaced weekly until female death. Consistent with expectations3-5, we found that females exposed to AAA-males had significantly higher lifetime reproductive success than females exposed to ABC-males (Fig. 1a). This was due to the fact that while total female lifespan did not differ on average between treatments (F 1, 119 = 1.66, P = 0.2), females exposed to AAA-males had significantly longer reproductive lifespan (from eclosion to last egg-laying day6, Fig. 1b), and female reproductive lifespan was positively correlated with female lifetime reproductive success (F 1, 117 = 484.59, P < 0.001). Two non-mutually exclusive mechanisms might cause this. First, high-fecundity females might die faster when exposed to ABC-males, leading to an average higher productivity of AAA-replicates ('selective death'). Second, individual Author contributions. Expt.1 was designed by P.C., S.W. and T.P., conducted by P.C. and F.A. and analysed by P.C. Expt. 2 was designed by P.C., C.K.W.T., S.W. and T.P., and conducted/analysed by P.C. Expt. 3 was designed and conducted by S.W. and P.C. and analysed by P.C. Expt. 4 was designed by C.K.W.T., T.P. and S.W., and conducted/analysed by C.K.W.T. The article was conceived and written by T.P. with input from P.C., C.K.W.T. and S.W. Europe PMC Funders Author Manuscripts females might suffer a steeper rate of age-dependent decline in reproductive output when exposed...
Female promiscuity can generate postcopulatory competition among males, but it also provides the opportunity for exploitation of rival male ejaculates. For example, in many insect species, male seminal fluid proteins (Sfps) transferred in a female's first mating stimulate increased fecundity and decreased receptivity to remating. Subsequent mates of females could potentially take advantage of the effects of the first male's Sfps and strategically reduce investment in their own ejaculate. We compared postmating responses (fecundity and sexual receptivity) of Drosophila melanogaster females after their first (virgin) matings (V), to the responses of females remating (M) 24 h after their first mating. The results show that M matings fail to boost fecundity and, thus, males are unlikely to gain fitness from transferring Sfps whose sole function-in V matings-is fecundity-stimulation. However, males can protect their likelihood of paternity in M matings through the transfer of receptivity-inhibiting Sfps. The levels of a fecundity-stimulating Sfp (ovulin) were significantly lower in M females relative to V females, at the same time point shortly after the end of mating. In contrast, the levels of a key receptivityinhibiting Sfp (sex peptide) were the same in M and V females. These results support the hypothesis that males can adaptively tailor the composition of proteins in the ejaculate, allowing a male to take advantage of the fecundity-stimulating effects of the previous male's ovulin, yet maintaining investment in sex peptide. Furthermore, our results demonstrate sophisticated protein-specific ejaculate manipulation. strategic ejaculation | male accessory gland | sexual selection | intersexual interaction | reproduction F emale sexual promiscuity creates an arena for sperm competition and other forms of postcopulatory sexual selection (1, 2). Promiscuity may also provide the opportunity for males to exploit the effects of rival males' ejaculates (3, 4). This opportunity arises because, in many species, the ejaculate not only is essential for fertilization but also can influence female postmating behavior and physiology in ways that promote male reproductive success. For example, in insects, products of the male accessory glands can have a variety of effects in the mated female, including stimulating fecundity, promoting sperm storage, and inhibiting receptivity to remating (reviewed in refs. 5-8). In mammals, functions of seminal fluids in the mated female can include stimulating ovulation, promoting sperm motility, mediating sperm storage, and protecting sperm through suppression of immune defense (9, 10; reviewed in ref. 11). If these maleinduced effects persist beyond the time by which a female remates, then her next mate could exploit the effects of her earlier mates' ejaculates. A male could thereby reduce his own mating costs by decreasing investment in particular components of his own ejaculate.Recently developed theoretical models make specific predictions about ejaculate exploitation. For example, Hodgson...
Postcopulatory sexual selection (PCSS), comprised of sperm competition and cryptic female choice, has emerged as a widespread evolutionary force among polyandrous animals. There is abundant evidence that PCSS can shape the evolution of sperm. However, sperm are not the whole story: they are accompanied by seminal fluid substances that play many roles, including influencing PCSS. Foremost among seminal fluid models is Drosophila melanogaster , which displays ubiquitous polyandry, and exhibits intraspecific variation in a number of seminal fluid proteins (Sfps) that appear to modulate paternity share. Here, we first consolidate current information on the identities of D. melanogaster Sfps. Comparing between D. melanogaster and human seminal proteomes, we find evidence of similarities between many protein classes and individual proteins, including some D. melanogaster Sfp genes linked to PCSS, suggesting evolutionary conservation of broad-scale functions. We then review experimental evidence for the functions of D. melanogaster Sfps in PCSS and sexual conflict. We identify gaps in our current knowledge and areas for future research, including an enhanced identification of PCSS-related Sfps, their interactions with rival sperm and with females, the role of qualitative changes in Sfps and mechanisms of ejaculate tailoring. This article is part of the theme issue ‘Fifty years of sperm competition’.
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