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Abstract:
Anopheles gambiae mosquitoes are major African vectors of
malaria, a disease that kills more than 600,000 people every year.
Given the spread of insecticide resistance in natural mosquito populations,
alternative vector control strategies aimed at reducing
the reproductive success of mosquitoes are being promoted. Unlike
many other insects, An. gambiae females mate a single time in
their lives and must use sperm stored in the sperm storage organ,
the spermatheca, to fertilize a lifetime’s supply of eggs. Maintenance
of sperm viability during storage is therefore crucial to the
reproductive capacity of these mosquitoes. However, to date, no
information is available on the factors and mechanisms ensuring
sperm functionality in the spermatheca. Here we identify cellular
components and molecular mechanisms used by An. gambiae
females to maximize their fertility. Pathways of energy metabolism,
cellular transport, and oxidative stress are strongly regulated
by mating in the spermatheca. We identify the mating-induced
heme peroxidase (HPX) 15 as an important factor in long-term
fertility, and demonstrate that its function is required during
multiple gonotrophic cycles. We find that HPX15 induction is
regulated by sexually transferred 20-hydroxy-ecdysone (20E), a
steroid hormone that is produced by the male accessory glands
and transferred during copulation, and that expression of this
peroxidase is mediated via the 20E nuclear receptor. To our knowledge,
our findings provide the first evidence of the mechanisms
regulating fertility in Anopheles, and identify HPX15 as a target
for vector control.