An Ectopic Expression Screen Reveals the Protective and Toxic Effects of Drosophila Seminal Fluid Proteins

Abstract

In Drosophila melanogaster, seminal fluid regulates the reproductive and immune responses of mated females. Some seminal fluid proteins may provide protective functions to mated females, such as antimicrobial activity and/or stimulation of antimicrobial gene expression levels, while others appear to have negative effects, contributing to a ''cost of mating.'' To identify seminal proteins that could participate in these phenomena, we used a systemic ectopic expression screen to test the effects on unmated females of proteins normally produced by the male accessory gland (Acps). Of the 21 ectopically expressed Acps that we tested for ability to assist in the clearance of a bacterial infection with Serratia marcescens, 3 Acps significantly reduced the bacterial counts of infected females, suggesting a protective role. Of the 23 Acps that we tested for toxicity, 3 were toxic, including one that has been implicated in the cost of mating in another study. We also tested ectopic expression females for other Acp-induced effects, but found no additional Acps that affected egg laying or receptivity upon ectopic expression.

Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: Potential tools for control of female feeding and reproduction

“…This pattern is similar to that found within the Drosophila genus: in a comparison across 12 Drosophila species Haerty et al (In press) found far fewer homologs of D. melanogaster mRGPs than of non-mRGPs. Mueller et al, 2007). All seven protease inhibitors we identified include predicted serine protease inhibitor (serpin) domains.…”

“…In D. melanogaster, several Acps have been found to have either direct antimicrobial activity or to modulate a female's ability to fight infection (Samakovlis et al, 1991;Lung et al, 2001;Mueller et al, 2007). Several putative Ae.…”

“…aegypti have been attributed to the effect of specific mRGPs in another Diptera species, Drosophila melanogaster (reviewed in Wolfner, 2002;Gillott, 2003;Chapman and Davies, 2004;Wolfner et al, 2005;Wong et al, 2006;. These proteins include: (1) simple peptides, including a "sex peptide" (Acp70A) that induces sexual refractoriness, increases the rate of egg production, and changes the feeding behavior and longevity of female Drosophila (Chapman et al, 2003;Liu and Kubli, 2003;Wigby and Chapman, 2005;Carvalho et al, 2006); (2) "prohormone-like" peptides, one of which (ovulin/Acp26Aa) stimulates ovulation (Heifetz et al, 2000); (3) large glycoproteins which are important for sperm storage (Neubaum and Wolfner, 1999) and other sperm-binding proteins; and (4) proteolysis regulators (Mueller et al, 2004;Ravi Ram et al, 2006;Mueller et al, 2007). Proteins synthesized in the male reproductive tract also have been found to play a role in regulating female post-mating physiology in a broad representation of other arthropods, including muscoid flies (Nelson et al, 1969), moths (Park et al, 1998), and ticks (Weiss and Kaufman, 2004).…”

Large Neurological Component to Genetic Differences Underlying Biased Sperm Use in Drosophila

“…While the ultimate outcome of a sperm competition depends on a complex interaction between male and female factors, the sexes often have different interests. Males are essentially in competition with other males, and while natural selection drives males to become better competitors with each other, it may result in males damaging the female through toxicity of seminal proteins (Wigby and Chapman 2004;Mueller et al 2007). On the other hand, females benefit from simply being able to produce the most and highest-fitness offspring, and this may entail a specific response to male-produced molecules that influence sperm competition.…”

Sex Peptide Is Required for the Efficient Release of Stored Sperm in Mated Drosophila Females

“…Sperm and SFPs influence the mated female's egg production and her sexual receptivity to subsequent males in two distinct phases: within the first 24 hr of mating (the ''short-term response,'' or STR), where increased egg production and reduced sexual receptivity depend on the receipt of SFPs (Kalb et al 1993;Xue and Noll 2000;Bretman et al 2010), and beyond 24 hr, when the maintenance of these processes requires both sperm and SFPs (the ''long-term response,'' or LTR; Manning 1962Manning , 1967Kalb et al 1993;Chapman et al 2003;Liu and Kubli 2003;Peng et al 2005a). In particular, the sex peptide (SP; Acp70A), a 36-amino-acid SFP, plays a central role in the LTR (reviewed in Kubli 2003;Ravi Ram and Wolfner 2007a;Chapman 2008), increasing egg production (Soller et al 1999) and decreasing female receptivity to remating (Chen et al 1988;Chapman et al 2003;Liu and Kubli 2003); SP also affects other behaviors and hormonal physiology (Moshitzky et al 1996;Peng et al 2005b;Wigby and Chapman 2005;Carvalho et al 2006;Mueller et al 2007;Isaac et al 2010). …”