Altered circadian rhythm, sleep, and rhodopsin 7-dependent shade preference during diapause in Drosophila melanogaster

TitleAltered circadian rhythm, sleep, and rhodopsin 7-dependent shade preference during diapause in Drosophila melanogaster
Publication TypeJournal Article
Year of Publication2024
AuthorsMeyerhof GT, Easwaran S, Bontempo AE, Montell C, Montell DJ
JournalProc Natl Acad Sci U S A
Volume121
Issue27
Paginatione2400964121
Date Published2024 Jul 02
ISSN1091-6490
KeywordsAnimals, Circadian Rhythm, Diapause, Insect, Drosophila melanogaster, Drosophila Proteins, Light, Photoperiod, Rhodopsin, Sleep, Temperature
Abstract

To survive adverse environments, many animals enter a dormant state such as hibernation, dauer, or diapause. Various species undergo adult reproductive diapause in response to cool temperatures and/or short day-length. While flies are less active during diapause, it is unclear how adverse environmental conditions affect circadian rhythms and sleep. Here we show that in diapause-inducing cool temperatures, exhibit altered circadian activity profiles, including severely reduced morning activity and an advanced evening activity peak. Consequently, the flies have a single activity peak at a time similar to when nondiapausing flies take a siesta. Temperatures ≤15 °C, rather than photoperiod, primarily drive this behavior. At cool temperatures, flies rapidly enter a deep-sleep state that lacks the sleep cycles of flies at higher temperatures and require high levels of stimulation for arousal. Furthermore, we show that at 25 °C, flies prefer to siesta in the shade, a preference that is virtually eliminated at 10 °C. Resting in the shade is driven by an aversion to blue light that is sensed by Rhodopsin 7 outside of the eyes. Flies at 10 °C show neuronal markers of elevated sleep pressure, including increased expression of Bruchpilot and elevated Ca in the R5 ellipsoid body neurons. Therefore, sleep pressure might overcome blue light aversion. Thus, at the same temperatures that cause reproductive arrest, preserve germline stem cells, and extend lifespan, are prone to deep sleep and exhibit dramatically altered, yet rhythmic, daily activity patterns.

DOI10.1073/pnas.2400964121
Alternate JournalProc Natl Acad Sci U S A
PubMed ID38917005
PubMed Central IDPMC11228485
Grant ListF31EY033179 / / HHS | NIH | National Eye Institute (NEI) /
R01DC016278 / / HHS | NIH | National Institute on Deafness and Other Communication Disorders (NIDCD) /
R01AG36907 / / HHS | NIH | National Institute on Aging (NIA) /
R01 AI169386 / AI / NIAID NIH HHS / United States
F31 EY033179 / EY / NEI NIH HHS / United States
R01AI169386 / / HHS | NIH | NIAID | Division of Intramural Research (DIR, NIAID) /
R01 EY008117 / EY / NEI NIH HHS / United States
R01EY008117 / / Joint Shantou International Eye Center (JSIEC) /
R01 DC016278 / DC / NIDCD NIH HHS / United States
F31 DC021112 / DC / NIDCD NIH HHS / United States