Fertility decline in female mosquitoes is regulated by theorcoolfactory co-receptor

Abstract

Female Aedes aegypti mosquitoes undergo multiple rounds of reproduction, known as gonotrophic cycles. These cycles span the period from blood meal intake to oviposition. Understanding how reproductive success is maintained across gonotrophic cycles allows for the identification of molecular targets to reduce mosquito population growth. Odorant receptor co-receptor (orco) encodes a conserved insect-specific transmembrane ion channel that complexes with tuning odorant receptors (ORs) to form a functional olfactory receptor. orco expression has been identified in the male and female mosquito germline, but its role is unclear. We report an orco-dependent, maternal effect reduction in fertility after the first gonotrophic cycle. This decline was rescued by repairing the orco mutant locus. Eggs deposited by orco mutant females are fertilized but the embryos reveal developmental defects, reduced hatching, and changes in ion channel signaling gene transcription. We present an unexpected role for an olfactory receptor pathway in mosquito reproduction.

Fertility decline inAedesmosquitoes is associated with reduced maternal transcript deposition and does not depend on female age

“…We previously reported a maternal effect decline in Ae. aegypti mosquito fertility associated with changes in the transcriptome of early embryos that resulted from the mutation of an olfactory coreceptor gene, orco [3]. Here, we provide evidence for the role of additional maternal gene products in sustaining mosquito fertility over multiple reproductive cycles.…”

“…Given our previous report that Ae. aegypti females store sperm that could last them more than three rounds of reproduction, and that over 90% of eggs laid in the second gonotrophic cycle are fertilized [3], it is unlikely that the fertility decline was due to sperm deficiency. Rather, we propose that a reduced deposition of key maternal gene products during oogenesis could negatively impact on embryonic development and/or hatching.…”

“…Transcriptomic data processing and analysis RNA sequencing (RNA-seq) data for 1-2hrs old wild-type Ae. aegypti embryos was retrieved from the transcriptome reported in our previous study [3]. Each library read was trimmed to remove adapter sequence and then mapped to gene models from AaegL5.0 genome [39,40].…”

“…Our previous study showed a fecundity and fertility decline between the first and second gonotrophic cycles in Ae. aegypti mosquitoes [3]. To determine if this phenotype is progressive and/or specific to Ae.…”

“…Pre-zygotic transition Ae. aegypti embryo gene expression analysis showed transcriptional changes cluster by gonotrophic cycle [3], suggesting that maternal mRNA deposited during oocyte development may vary between reproductive cycles. To gain better understanding into this hypothesis, we analyzed our transcriptomic data to identify changes in maternal gene expression profile between the first and second gonotrophic cycle Ae.…”