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

Abstract

Significance Anopheles gambiae females are the principal vectors of malaria, a disease that kills more than 600,000 people every year. Current control methods using insecticides to kill mosquitoes are threatened by the spread of resistance in natural populations. A promising alternative control strategy is based on interfering with mosquito reproduction to reduce the number of malaria-transmitting females. Here we show that a male hormone transferred to the female during sex induces large changes in female behavior. These changes, defined as the postmating switch, include a physical incapacity for fertilization by additional males and the ability to lay mature eggs. Tampering with the function of this hormone generates unprecedented opportunities to reduce the reproductive success of Anopheles mosquitoes and impact malaria transmission.

Evolution of sexually-transferred steroids inAnophelesmosquitoes

“…gambiae mosquitoes (14). Similarly to results obtained for the two post-mating responses analysed in this study, female monoandry (insemination by a single male) occurs in species whose males produce steroids but also in ones whose males do not (37)(38)(39)(40).…”

“…These differences are independent of males' ability to produce and transfer steroids to females and not correlated to malaria vectorial capacity (summarised in Table 1). Apart from follicle detachment, increase in egg development and induction of refractoriness to mating, numerous other functions of steroids have been described in adult insects (14,15,(48)(49)(50)(51)(52)(53). Thus, sexually-transferred steroids could mediate different functions with more or less direct benefit for the female's reproduction in Cellia females, due to the rapid evolution of reproductive systems between species.…”

“…gambiae mated females (14). A report further suggested that production of steroids by male Anopheles mosquitoes, their transfer to females during mating and mating-induced phenotypes would be specific to dominant human malaria vectors, likely determining these mosquito species' ability to transmit malaria to humans (15,16).…”

A comparative analysis of reproductive biology of insect vectors of human disease

“…The male triggers of monandry have been recently identified in An. gambiae : high titers of the steroid hormone 20-hydroxyecdysone (20E) transferred to the female atrium (uterus) within the mating plug contribute to switching the female to a mated status, rendering her refractory to further copulation (among other physiological changes – see below)[10]. As discussed later, both 20E and its precursor ecdysone (E) are also produced by the female after a blood meal, where they are essential for egg development.…”

“…In An. gambiae once again the male-transferred 20E has recently been identified as both a necessary and sufficient trigger of oviposition [10]: 38% of females that were mated to males with experimentally reduced 20E levels were not able to lay their eggs compared to 14% of females mated to control males; consistently, oviposition was stimulated in virgin blood-fed females by the injection of 20E in a dose-dependent manner [10]. 20E also regulates fertility over multiple blood feedings preserving sperm function by up-regulating a spermathecal detoxifying enzyme, the heme peroxidase HPX15, and possible other mechanisms [42].…”