Endocrine Regulation of Lifespan in Insect Diapause

Abstract

Diapause is a physiological adaptation to conditions that are unfavorable for growth or reproduction. During diapause, animals become long-lived, stress-resistant, developmentally static, and non-reproductive, in the case of diapausing adults. Diapause has been observed at all developmental stages in both vertebrates and invertebrates. In adults, diapause traits weaken into adaptations such as hibernation, estivation, dormancy, or torpor, which represent evolutionarily diverse versions of the traditional diapause traits. These traits are regulated through modifications of the endocrine program guiding development. In insects, this typically includes changes in molting hormones, as well as metabolic signals that limit growth while skewing the organism’s energetic demands toward conservation. While much work has been done to characterize these modifications, the interactions between hormones and their downstream consequences are incompletely understood. The current state of diapause endocrinology is reviewed here to highlight the relevance of diapause beyond its use as a model to study seasonality and development. Specifically, insect diapause is an emerging model to study mechanisms that determine lifespan. The induction of diapause represents a dramatic change in the normal progression of age. Hormones such as juvenile hormone, 20-hydroxyecdysone, and prothoracicotropic hormone are well-known to modulate this plasticity. The induction of diapause—and by extension, the cessation of normal aging—is coordinated by interactions between these pathways. However, research directly connecting diapause endocrinology to the biology of aging is lacking. This review explores connections between diapause and aging through the perspective of endocrine signaling. The current state of research in both fields suggests appreciable overlap that will greatly contribute to our understanding of diapause and lifespan determination.

Altered circadian rhythm, sleep, andrhodopsin 7-dependent shade preference during diapause inDrosophila melanogaster

“…The effects of cool temperatures on sleep and activity that we report here are also independent of the hormone JH, which is a key regulator of diapause that promotes vitellogenesis (1,8). We previously found that cool temperatures also arrest germline stem cell division independently of JH (13).…”

Female reproductive dormancy in Drosophila is regulated by DH31-producing neurons projecting into the corpus allatum

“…Diapause has been intensively studied in insects as its control could benefit many aspects of industry and agriculture ( Denlinger, 2008 , 2022 ; Denlinger et al, 2012 ). Previous studies have revealed that a fraction of insects enter diapause at the adult stage under diapause-inducing conditions, leading to multiple metabolic and behavioral changes, including slowed or halted reproductive maturation known as reproductive diapause ( Denlinger, 2022 ; Hutfilz, 2022 ; Kurogi et al, 2021 ). As female insect adults allocate extensive energy resources toward oogenesis ( Wheeler, 2003 ), reproductive diapause allows them to reduce their energy consumption and then resume reproduction under more favorable conditions.…”

A genome-wide association study implicates the olfactory system inDrosophila melanogasterdiapause-associated lifespan extension and fecundity

“…However, it has become clear that diapause is a comprehensive program that changes virtually every aspect of the fly’s life from behavior and to metabolism, reproduction, and lifespan (Tatar and Yin 2001; Kubrak et al 2014; Denlinger 2023). Prior studies have identified temperature and day-length as relevant environmental cues and key hormonal regulators such as insulin, juvenile hormone (JH), and 20-hydroxyecdysone (20E), which coordinate metabolism and reproduction (Hutfilz 2022; Denlinger 2023). Recent studies identify specific circadian neurons that sense changes in temperature and relay that information to the reproductive system (Meiselman et al 2022; Hidalgo et al 2023).…”