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Review
. 2022 Apr 25:16:778264.
doi: 10.3389/fnbeh.2022.778264. eCollection 2022.

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

Affiliations
Review

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

In Hae Lee et al. Front Behav Neurosci. .

Abstract

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.

Keywords: Ae. albopictus; diapause; mosquito; reproduction; seasonal change.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Aedes albopictus global invasion and population expansion in temperate and tropical regions. (A) Global map of predicted distribution of Ae. albopictus population (adapted from Kraemer et al., 2015). Adult females found in tropical regions lay non-diapause eggs (magenta) majority of year-round. In temperate regions, adult females found in favorable conditions (magenta) lay non-diapause eggs. In unfavorable conditions, adult females alter their reproduction (blue) and lay diapause eggs (blue). (B) Incidence of Ae. albopictus at different life stages in temperate regions. Temperate population have unique subsets of developmental stages present (diapause and non-diapause egg, larva, pupa, adult) in each season. Incidence of adult Ae. albopictus in temperate region is depicted by the gradient graph.
FIGURE 2
FIGURE 2
Clock cells in diapausing and non-diapausing insects. (A) Model for environmental inputs to predicted clock cell subgroups in Ae albopictus that are candidates for regulating diapause entry in adult females. Light and temperature cues are detected by central brain clock cells expressing the neuropeptide Pigment Dispersing Factor (PDF) shown in purple and/or core clock genes (denoted by period (per) in teal). Predicted clock subgroups are based on observations in D. melanogaster and Ae. aegypti (Baik et al., 2020). (B) Insects with no/weak diapause and those with adult female diapause (C) show conservation of clock anatomy, including distinct subgroups of central brain cells that express combination of per and PDF.
FIGURE 3
FIGURE 3
Multi-organ signaling pathways for maternally instigated diapause in female Ae. Albopictus. Environmental cues such as photoperiod and temperature are sensed by the central brain and signal the fat body using (1) ILPs (insulin-like peptides) and (2) juvenile hormone released by the corpora allata (CA). ILPs bind to insulin receptor and activate FOXO pathway. Blood nutrients are digested by the midgut and the integration of environmental cue and blood-fed status trigger the release of vitellogenin and 20E signaling to the ovaries to alter reproduction in diapause state. 20E feedback to the fat body and is likely to affect juvenile hormone biosynthesis.

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