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

Abstract

To survive adverse environments, many animals enter a dormant state such as hibernation, dauer, or diapause. Various Drosophila species undergo adult reproductive diapause in response to cool temperatures and/or short day-length. While it is known that flies are less active during diapause, an in-depth understanding of diapause effects on circadian rhythms and sleep is lacking. Here we show that, in diapause-inducing conditions, Drosophila melanogaster exhibit altered circadian activity profiles, including a severely reduced morning activity peak and an advanced evening activity peak. Consequently, the flies have a single activity peak at a time similar to when non-diapausing flies have a siesta. Temperatures [≤]15 {degrees}C, rather than short day-length, primarily drive the behavior. At cool temperatures, flies also rapidly enter a deep sleep state that lacks the sleep cycles of flies at higher temperatures and requires particularly high levels of stimulation for arousal. Furthermore, we show that at 18-25 {degrees}C, flies prefer to siesta in the shade, a preference that is virtually eliminated at 10 {degrees}C. Resting in the shade is driven by an aversion to blue light, sensed by rhodopsin 7 (Rh7) outside of the eyes. Flies at 10 {degrees}C show neuronal markers of elevated sleep pressure, including increased expression of Bruchpilot and elevated Ca2+ in the R5 ellipsoid body neurons. Therefore sleep pressure might overcome blue light aversion. Thus at temperatures known to cause reproductive arrest, preserve germline stem cells, and extend lifespan, Drosophila melanogaster are prone to deep sleep and exhibit dramatically altered - yet rhythmic - daily activity patterns. Significance statementClimate change is impacting many animals, including insects. In diverse organisms, adverse environments trigger dormancy programs such as hibernation and diapause. Fruit flies undergo diapause to survive winter. Here we develop new methods and show that the same cool temperatures that delay fruit fly reproduction and extend lifespan, also promote deep sleep. Cool flies rapidly fall asleep and are difficult to arouse. Once awake, they immediately fall back to sleep. Whereas in warm environments, midday blue light drives flies to siesta in the shade, in cool temperatures the need to sleep overwhelms light-aversion, reducing shade preference. Animals that adjust their behavior directly to temperature, rather than day length, may be more resilient to a changing climate.