Abstract
Animals maximize fitness by modulating sleep and foraging strategies in response to changes in nutrient availability. Wild populations of the fruit fly, Drosophila melanogaster, display highly variable levels of starvation and desiccation resistance that differ in accordance with geographic location, nutrient availability, and evolutionary history. Further, flies potently modulate sleep in response to changes in food availability, and selection for starvation resistance enhances sleep, revealing strong genetic relationships between sleep and nutrient availability. To determine the genetic and evolutionary relationship between sleep and nutrient deprivation, we assessed sleep in flies selected for desiccation or starvation resistance. While starvation resistant flies have higher levels of triglycerides, desiccation resistant flies have enhanced glycogen stores, indicative of distinct physiological adaptations to food or water scarcity. Strikingly, selection for starvation resistance, but not desiccation resistance, leads to increased sleep, indicating that enhanced sleep is not a generalized consequence of higher energy stores. Thermotolerance is not altered in starvation or desiccation resistant flies, providing further evidence for context-specific adaptation to environmental stressors. F2 hybrid flies were generated by crossing starvation selected flies with desiccation selected flies, and the relationship between nutrient deprivation and sleep was examined. Hybrids exhibit a positive correlation between starvation resistance and sleep, while no interaction was detected between desiccation resistance and sleep, revealing that prolonged sleep provides an adaptive response to starvation stress. Therefore, these findings demonstrate context-specific evolution of enhanced sleep in response to chronic food deprivation, and provide a model for understanding the evolutionary relationship between sleep and nutrient availability.
Highlights
Sleep is a near universal animal behavior, with highly conserved functional and molecular properties [1,2]
We found that triglyceride levels are significantly higher in all three groups of SR flies compared to FSR control flies, while no difference was observed between desiccation resistance (DR) selected flies and FDR controls, indicating that only selection for starvation resistance results in increased triglyceride accumulation (Fig 1C and S1 Fig)
For Group A, free glucose is elevated in SR and reduced in DR selected groups compared to controls, indicating that selection primarily effects triglyceride energy stores in this group (Fig 1E and S1 Fig)
Summary
Sleep is a near universal animal behavior, with highly conserved functional and molecular properties [1,2]. While sleep is clearly influenced by many environmental factors, sleep timing and duration are closely related to nutrient availability and foraging strategy [8,9]. Both flies and mammals suppress sleep in response to starvation, presumably in order to forage for food. This indicates a functional trade-off between sleep duration and feeding [7,10,11]. There are likely evolutionary interactions between sleep and nutrient availability, these interactions are not well understood
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