Abstract
Regulation of sleep and metabolic homeostasis is critical to an animal's survival and under stringent evolutionary pressure. Animals display remarkable diversity in sleep and metabolic phenotypes; however, an understanding of the ecological forces that select for, and maintain, these phenotypic differences remains poorly understood. The fruit fly, Drosophila melanogaster, is a powerful model for investigating the genetic regulation of sleep and metabolic function, and screening in inbred fly lines has led to the identification of novel genetic regulators of sleep. Nevertheless, little is known about the contributions of naturally occurring genetic differences to sleep, metabolic phenotypes, and their relationship with geographic or environmental gradients. Here, we quantified sleep and metabolic phenotypes in 24 D. melanogaster populations collected from diverse geographic localities. These studies reveal remarkable variation in sleep, starvation resistance, and energy stores. We found that increased sleep duration is associated with proximity to the equator and elevated average annual temperature, suggesting that environmental gradients strongly influence natural variation in sleep. Further, we found variation in metabolic regulation of sleep to be associated with free glucose levels, while starvation resistance associates with glycogen and triglyceride stores. Taken together, these findings reveal robust naturally occurring variation in sleep and metabolic traits in D. melanogaster, providing a model to investigate how evolutionary and ecological history modulate these complex traits.
Highlights
Species display robust differences in homeostatically regulated behaviors including sleep, feeding, and metabolic function, yet little is known about the ecological and functional relationship between these traits (Aulsebrook, Jones, Rattenborg, Roth, & Lesku, 2016; Eban-Rothschild, Giardino, & de Lecea, 2017)
Inspired by previous work investigating the relationship between geographic locality and sleep regulation (Svetec et al, 2015), we examined the relationship between sleep, metabolic function, and environmental localities
We describe the analysis of sleep regulation, starvation resistance, the effects of starvation on sleep, and measurements of nutrient storage in D. melanogaster collected from geographically distinct localities that differ in latitude, longitude, temperature, and altitude to determine the environmental and geographic factors that associate with sleep regulation
Summary
Species display robust differences in homeostatically regulated behaviors including sleep, feeding, and metabolic function, yet little is known about the ecological and functional relationship between these traits (Aulsebrook, Jones, Rattenborg, Roth, & Lesku, 2016; Eban-Rothschild, Giardino, & de Lecea, 2017). Sleep is measured by 5 min of inactivity because it correlates with all other characteristics of sleep (Shaw, Cirelli, Greenspan, & Tononi, 2000) Flies acutely modulate their sleep in accordance with nutrient availability, and starvation potently inhibits sleep and initiates foraging, thereby providing a system to investigate the relationship between sleep and metabolic regulation (Keene et al, 2010; Lee & Park, 2004; Linford, Chan, & Pletcher, 2012). Selection for short-sleeping flies results in reduced energy stores and sensitivity to starvation, while selecting for starvation resistance increases sleep duration (Masek et al, 2014; Seugnet et al, 2009) These studies have provided insight into the genetic and functional relationship between sleep and metabolic regulation; yet, the ecological factors that shape the diversity of these traits, such as temperature, lighting, humidity, and distribution of food resources in naturally occurring populations remain poorly understood. Our findings reveal highly significant variation in all traits measured, suggesting these traits are influenced by their environmental and evolutionary history
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