Insulin-like peptides regulate oogenesis by stimulating ovarian ecdysteroid production in the Indian malaria mosquitoAnopheles stephensi

Abstract

AbstractFemales of many mosquito species feed on vertebrate blood to produce eggs, making them effective disease vectors. In the dengue vectorAedes aegypti, blood feeding signals the brain to release ovary ecdysteroidogenic hormone (OEH) and insulin-like peptides (ILPs) that trigger ecdysteroid production by the ovaries. These ecdysteroids regulate synthesis of the yolk protein vitellogenin (Vg) that is packaged into eggs. Less is known about the reproductive biology ofAnophelesmosquitoes, which pose a greater public health threat thanAedesspp. because they are competent to transmit mammalian malaria. ILPs can triggerAn. stephensiovaries to secrete ecdysteroids. UnlikeAe. aegypti,Anophelesalso transfer ecdysteroids fromAnophelesmales to females during mating. To elucidate the role of OEH and ILPs inAn. stephensi, we decapitated blood-fed females to ablate the source of these peptides and injected them with each hormone. Yolk deposition into oocytes was abolished in decapitated females and rescued by ILP injection. ILP activity was dependent on blood feeding and little change in triglyceride and glycogen stores was observed in response to blood-feeding, suggesting this species requires nutrients from blood to form eggs. We also measured egg maturation, ecdysteroid titers, and yolk protein expression in mated and virgin females. Although yolk deposition into developing oocytes was significantly reduced in virgins compared to mated females, no differences in ecdysteroid titers or Vg transcript abundance were detected between these groups. 20-hydroxyecdysone (20E) stimulated Vg expression in female fat bodies in primary culture. Given these results, we conclude that ILPs control egg formation by regulating ecdysteroid production in the ovaries.