The fate of follicles after a blood meal is dependent on previtellogenic nutrition and juvenile hormone in Aedes aegypti

Juvenile hormone (JH) mediates the relationship between fecundity and nutrition during the gonotrophic cycle of the mosquito in three ways: (1) by regulating initial previtellogenic development, (2) by mediating previtellogenic resorption of follicles and (3) by altering intrinsic previtellogenic follicle “quality”, physiology, and competitiveness thereby predetermining the fate of follicles after a blood meal. To support a role for JH in mediating the response of ovarian follicles after a blood meal, we explored three main questions: (1) Do changes in nutrition during the previtellogenic resting stage lead to relevant biochemical and molecular changes in the previtellogenic ovary? (2) Do hormonal manipulations during the previtellogenic resting stage lead to the same biochemical and molecular changes? (3) Does nutrition and hormones during the previtellogenic resting stage affect vitellogenic resorption and reproductive output? We examined the accumulation of neutral lipids in the previtellogenic ovary as well as the previtellogenic expression of genes integral to endocytosis and oocyte development such as the: vitellogenin receptor (AaVgR), lipophorin receptor (AaLpRov), heavy-chain clathrin (AaCHC), and ribosomal protein L32 (rpL32) under various previtellogenic nutritional and hormonal conditions. mRNA abundance and neutral lipid content increased within the previtellogenic ovary as previtellogenic mosquitoes were offered increasing sucrose concentrations. Methoprene application mimicked the effect of offering the highest sucrose concentrations on mRNA abundance and lipid accumulation in the previtellogenic ovary. These same nutritional and hormonal manipulations altered the extent of vitellogenic resorption. Mosquitoes offered 20% sucrose during the previtellogenic resting stage had nearly 3 times less vitellogenic resorption than mosquitoes offered 3% sucrose despite taking smaller blood meals and developed ∼10% more eggs during the first gonotrophic cycle. Mosquitoes treated with JH III during the previtellogenic resting stage and then offered a blood meal had a ∼40% reduction in the amount of vitellogenic resorption and developed ∼12% more eggs. Taken together, these results suggest that previtellogenic nutrition alters the extent and pattern of resorption after a blood meal through the effect of JH on mRNA abundance and lipid accumulation in previtellogenic follicles.

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► The lipid content of the previtellogenic ovary reflects overall nutritional reserves.
► Accumulation of ovarian mRNA’s integral to oogenesis depend on nutrition and hormones.
► JH III treatment during the previtellogenic stage affects post blood meal resorption.
► Nutrition during the previtellogenic stage also affects post blood meal resorption.
► JH mediates reproductive output by affecting the follicles development potential.