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.摘要：昼夜节律钟（circadian clock）在地球上广泛分布，学界普遍认为其可为生物体赋予适应性优势。功能正常的昼夜节律钟及其与外部环境的同步作用，也被证实可为人类健康带来益处。然而，有关拥有昼夜节律钟所能带来的益处的实验证据仍较为匮乏，且目前大多仅局限于原核生物。本研究以黑腹果蝇（Drosophila melanogaster）为研究对象，为昼夜节律钟及时序化生命活动的益处提供了实验证据。研究结果显示，果蝇会主动选择并偏好处于受昼夜节律钟调控的环境中：持续光照会破坏果蝇的昼夜节律钟，使其运动活动呈现无节律模式。当在恒亮环境中为果蝇提供可在黑暗区域与光照区域间移动的选择时，果蝇能够维持甚至重新恢复节律性行为模式。这些节律与果蝇在两个区域间的规律性位置变化高度吻合，证明果蝇会主动营造有利于昼夜节律钟功能发挥与时序组织的生存环境。这种由果蝇自主产生的节律，与已知驱动果蝇行为节律的大多数时钟神经元的分子节律相匹配，证实这些行为节律确实由昼夜节律钟调控。最后，与无节律的果蝇相比，具备行为节律性的果蝇其睡眠节律得以恢复，且睡眠模式更为连贯。尽管生物体无需昼夜节律钟也可存活，但本研究证实，若赋予选择机会，动物会偏好以时序化方式生存，并主动营造这种生存条件。该研究为拥有并利用昼夜节律钟的益处提供了有力支撑，例如通过保障更高质量的睡眠。