Insect diapause: from a rich history to an exciting future

Abstract

Diapause, a stage-specific developmental arrest, is widely exploited by insects to bridge unfavorable seasons. Considerable progress has been made in understanding the ecology, physiology and evolutionary implications of insect diapause, yet intriguing questions remain. A more complete understanding of diapause processes on Earth requires a better geographic spread of investigations, including more work in the tropics and at high latitudes. Questions surrounding energy management and trade-offs between diapause and non-diapause remain understudied. We know little about how maternal effects direct the diapause response, and regulators of prolonged diapause are also poorly understood. Numerous factors that were recently linked to diapause are still waiting to be placed in the regulatory network leading from photoreception to engagement of the diapause program. These factors include epigenetic processes and small noncoding RNAs, and emerging data also suggest a role for the microbiome in diapause regulation. Another intriguing feature of diapause is the complexity of the response, resulting in a diverse suite of responses that comprise the diapause syndrome. Select transcription factors likely serve as master switches turning on these diverse responses, but we are far from understanding the full complexity. The richness of species displaying diapause offers a platform for seeking common components of a ‘diapause toolbox’. Across latitudes, during invasion events and in a changing climate, diapause offers grand opportunities to probe evolutionary change and speciation. At a practical level, diapause responses can be manipulated for insect control and long-term storage. Diapausing insects also contain a treasure trove of pharmacological compounds and offer promising models for human health.

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).…”

“…S2 A and B ; (12)]. Ovarian arrest during diapause is in part regulated by a reduction in juvenile hormone (JH) signaling (8, 32, 33). Treating flies with the JH analog Methoprene partially reverses this arrest, causing ovaries to enlarge [ SI Appendix , Fig.…”

“…Classically-studied diapause traits include slow growth and development, reproductive arrest, altered metabolism, increased stress resistance, and lifespan extension (2, 8). Less studied have been the effects of diapause-inducing conditions on behavior.…”

“…Many open questions remain (8). For example, an in-depth understanding of diapause effects on behavior, especially circadian rhythms and sleep characteristics, is lacking.…”

Tempo and mode of diapause evolution in butterflies

“…Apart from these sporadic examples (which also had a relatively low number of taxa), investigations of macroevolutionary dynamics of diapause evolution in animals, especially in insects, has not received much attention. In a recent commentary, Denlinger (2023) even acknowledged that "we still lack ambitious phylogenetic analyses that enable us to draw conclusions about the deep history of diapause". In this study, by capitalizing on the rich information on the natural history of butterflies, we provide insights into the tempo and mode of diapause evolution using a large number of taxa in a macroevolutionary framework.…”