Spermless males elicit large-scale female responses to mating in the malaria mosquito Anopheles gambiae

Abstract

Anopheles gambiae sensu stricto is the major vector of malaria, a disease with devastating consequences for human health. Given the constant spread of the disease, alternative approaches to the use of insecticides are urgently needed to control vector populations. Females of this species undergo large behavioral changes after mating, which include a life-long refractoriness to further insemination and the induction of egg laying in blood-fed individuals. Genetic control strategies aimed at impacting Anopheles fertility through the release of sterile males are being advocated to reduce the size of mosquito field populations. Such strategies depend on the ability of the released sterile males to mate successfully with wild females and to switch off the female receptivity to further copulation. Here we evaluate the role of sperm in regulating female behavioral responses after mating in An. gambiae. We developed spermless males by RNAi silencing of a germ cell differentiation gene. These males mated successfully and preserved standard accessory gland functions. Females mated to spermless males exhibited normal postcopulatory responses, which included laying large numbers of eggs upon blood feeding and becoming refractory to subsequent insemination. Moreover, spermless males induced transcriptional changes in female reproductive genes comparable to those elicited by fertile males. Our data demonstrate that, in contrast to Drosophila, targeting sperm in An. gambiae preserves normal male and female reproductive behavior for the traits and time frame analyzed and validate the use of approaches based on incapacitation or elimination of sperm for genetic control of vector populations to block malaria transmission.oviposition | reproduction | sexual refractoriness | postmating behavior | insect

Mating activates the heme peroxidase HPX15 in the sperm storage organ to ensure fertility in Anopheles gambiae

“…3), demonstrating that the matinginduced transcriptional response occurs in spermathecal cells. Moreover, these data suggest that transfer of sperm is not a trigger of the spermathecal transcriptional response, confirming previous findings that female postmating physiology is not modulated by sperm (24) and pointing at a prominent role for MAG secretions as triggers of transcriptional changes.…”

Morphological and morphometrical assessment of spermathecae of Aedes aegypti females

“…In addition to affecting female behaviour, the spermathecal fluid also participates on the maturation of the spermatozoa after mating (Giuffrida et al 1995). Besides spermatozoa, mosquito spermathecae also store proteins from male seminal fluid (Sirot et al 2008, Thailayil et al 2011. We speculate that in spite of the presence of a relatively thick spermathecal cuticle (0.7 µm) (Clements & Potter 1967) male proteins might be capable of reaching the haemolymph.…”

“…These changes in inseminated females appear to be induced by molecules produced in male accessory glands and transferred to the female during mating as suggested by Avila et al (2010) and recently confirmed for An. gambiae (Thailayil et al 2011). A catalogue containing 145 male-derived proteins was recently identified, some of which potentially associated with post-insemination behaviour effects (Sirot et al 2011).…”

Sexual transfer of the steroid hormone 20E induces the postmating switch in Anopheles gambiae

“…The An. gambiae postmating switch, on the other hand, does not seem to depend on sperm transfer, because females mated to spermless males are capable of laying eggs and do not mate again (11). A number of methodologies have been used to elucidate the triggers of egg-laying and monandry in these mosquitoes (12)(13)(14)(15); although these studies yield contrasting results, they suggest that the MAG secretions that compose the mating plug have a prominent role in regulating these responses.…”