Maternally Instigated Diapause in Aedes albopictus: Coordinating Experience and Internal State for Survival in Variable Environments

The Asian tiger mosquito, Aedes albopictus, is one of the most dangerous invasive species in the world. Females bite mammalian hosts, including humans, to obtain blood for egg development. The ancestral range of Ae. albopictus likely spanned from India to Japan and this species has since invaded a substantial portion of the globe. Ae. albopictus can be broadly categorized into temperate and tropical populations. One key to their ability to invade diverse ecological spaces is the capacity of females to detect seasonal changes and produce stress-resistant eggs that survive harsh winters. Females living in temperate regions respond to cues that predict the onset of unfavorable environmental conditions by producing eggs that enter maternally instigated embryonic diapause, a developmentally arrested state, which allows species survival by protecting the embryos until favorable conditions return. To appropriately produce diapause eggs, the female must integrate environmental cues and internal physiological state (blood feeding and reproductive status) to allocate nutrients and regulate reproduction. There is variation in reproductive responses to environmental cues between interfertile tropical and temperate populations depending on whether females are actively producing diapause vs. non-diapause eggs and whether they originate from populations that are capable of diapause. Although diapause-inducing environmental cues and diapause eggs have been extensively characterized, little is known about how the female detects gradual environmental changes and coordinates her reproductive status with seasonal dynamics to lay diapause eggs in order to maximize offspring survival. Previous studies suggest that the circadian system is involved in detecting daylength as a critical cue. However, it is unknown which clock network components are important, how these connect to reproductive physiology, and how they may differ between behavioral states or across populations with variable diapause competence. In this review, we showcase Ae. albopictus as an emerging species for neurogenetics to study how the nervous system combines environmental conditions and internal state to optimize reproductive behavior. We review environmental cues for diapause induction, downstream pathways that control female metabolic changes and reproductive capacity, as well as diapause heterogeneity between populations with different evolutionary histories. We highlight genetic tools that can be implemented in Ae. albopictus to identify signaling molecules and cellular circuits that control diapause. The tools and discoveries made in this species could translate to a broader understanding of how environmental cues are interpreted to alter reproductive physiology in other species and how populations with similar genetic and circuit organizations diversify behavioral patterns. These approaches may yield new targets to interfere with mosquito reproductive capacity, which could be exploited to reduce mosquito populations and the burden of the pathogens they transmit.

Automated summary

The Asian tiger mosquito, a dangerous invasive species, is capable of coordinating its reproductive behavior and producing stress-resistant eggs in response to environmental cues and internal physiological state. However, little is known about how the female mosquito detects environmental changes and lays diapause eggs for offspring survival.