Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster

Abstract

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...

Sperm wars and the evolution of male fertility

“…What is even more remarkable is that males appear able to tailor their seminal fluid composition to a particular mating event. Thus, when mating with a virgin female, males will transfer relatively more ovulin than when mating with a previously mated female, presumably because oviposition has already been induced by the female's previous mating partner (Sirot et al 2011). Such strategic adjustments in fecundity enhancing sfps are consistent with the predictions arising from game theoretic modeling of male ejaculate expenditure (Cameron et al 2007, Alonzo & Pizzari 2010.…”

Reproductive activity triggers accelerated male mortality and decreases lifespan: genetic and gene expression determinants in Drosophila

“…Accordingly, in Mediterranean flies, Ceratitis capitata, costs of male courtship were higher than reproduction-induced costs because of sperm production or mating (Papadopoulos et al, 2010). On the other hand, data from Drosophila and crickets point to their ability to modulate the composition of the ejaculate (Sirot et al, 2011;Dowling and Simmons, 2012), and potentially alter the allocation of reproductive costs. Nevertheless, observations of gamete production costs would need to be reconciled with data from worms indicating that removal of the somatic gonad compensates for removal of the germline (Kenyon, 2010).…”

“…These costs can themselves be modulated with age. For instance, female attributes and male age have been implicated in the modulation of sperm production costs (Sirot et al, 2011;Dowling and Simmons, 2012). Nevertheless, naturally occurring genetic variation in males and in females might limit the generality of studies that address molecular mechanisms of reproduction and longevity within a single genotype.…”

“…Mechanisms through which male-female interactions affect mortality and longevity are varied, and include: (1) a direct role of the germline in somatic aging (Hsin and Kenyon, 1999;Kirkwood and Austad, 2000;ArantesOliveira et al, 2002;Cargill et al, 2003;Ghazi et al, 2009;Austad, 2010;Kenyon, 2010;Tatar, 2010;Mason et al, 2011;McCormick et al, 2011;Gendron et al, 2014;Maures et al, 2014;Shi and Murphy, 2014), (2) male and female harm to each other during copulation (Chapman et al, 1995;Wolfner, 2009), (3) costs to gamete production (Sirot et al, 2011;Dowling and Simmons, 2012) and (4) observations of diffusible sex-harming factors transmitted between the sexes and between individuals of the same sex (Gendron et al, 2014;Maures et al, 2014;Shi and Murphy, 2014). These costs can themselves be modulated with age.…”

Sexual Conflict and Sperm Competition

“…By manipulating these female traits, males increase their fertilization success. Furthermore, it has been shown that male D. melanogaster strategically adjust allocation of seminal peptides in accordance with female mating status and the perceived risk of sperm competition (Wigby et al 2009;Fedorka et al 2011;Sirot et al 2011) as predicted by theory (Hodgson and Hosken 2006). However, male manipulation comes at a cost to females, as seminal fluid proteins reduce female longevity (Chapman et al 1995) and alter egg production schedules to reduce female lifetime reproductive success (Wigby and Chapman 2005).…”