Fruit flies actively restart their circadian clock by proactively shaping their environment

Abstract

Circadian clocks are prevalent on Earth and are generally believed to provide adaptive advantage to organisms. Functional circadian clocks, and their synchronization with the outside world, has also been implicated to provide health benefits for humans. However, experimental evidence for the benefits of possessing a circadian clock is sparse and largely restricted to prokaryotic organisms. Here, we provide evidence for the benefits of circadian clocks and temporally organized life in the fruit fly Drosophila melanogaster. We demonstrate that flies prefer and actively choose to live under circadian clock regulation: Exposure to constant light breaks down the circadian clock and leads to arrhythmic locomotor activity patterns. When given the choice to move between dark and illuminated areas in a constant light environment, flies were able to maintain, or even re-gain, rhythmic behavioural patterns. These rhythms were mirrored by regular positional changes between the two areas, demonstrating that flies actively contribute to creating an environment allowing circadian clock function and temporal organisation. The self-inflicted rhythms were accompanied by molecular rhythms in the majority of the clock neurons known to drive behavioural rhythms in flies, showing that they are indeed controlled by the circadian clock. Finally, behavioural rhythmicity was correlated with restoration of rhythmic sleep patterns and less-fragmented sleep compared to arrhythmic flies. While life is possible without a circadian clock, we show that if given the choice, animals prefer to live in a temporally organized manner and actively contribute to make this possible. This provides strong arguments for the benefits of possessing and using a circadian clock, for example by ensuring a better quality of sleep.