Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production

Many insects are able to adjust their egg production according to physiological conditions such as nutrient supply and mating success. One way in which this is achieved is by resorption of some, or all, of the ovarian follicles at some stage during oogenesis. We have shown that the mosquito Anopheles stephensi responds in this manner when ookinetes of the malaria parasite Plasmodium yoelii nigeriensis first begin to invade the midgut. Little is known about the initiation and regulation of follicle resorption in any insect. Here, we demonstrate that there is a significant positive correlation between follicle resorption and the presence of follicular epithelial cells that are undergoing apoptosis. The parasite causes significantly more follicles to contain apoptotic cells from 16h post-infection onwards. Injection of a caspase inhibitor immediately after feeding on an infective blood meal prevents parasite-induced resorption of follicles and thus demonstrates that apoptosis precedes resorption. Ultrastructural studies show that patches of follicular epithelial cells contain condensed nuclear chromatin, a characteristic of apoptosis, and that no patency develops in these cells. Our work suggests that apoptosis plays a role in malaria-initiated inhibition of mosquito oogenesis and that caspase is central to this process. Follicle resorption is one of the main factors contributing to malaria-induced fecundity reduction in mosquitoes.