Altered regulation of sleep and feeding contribute to starvation resistance in <i>Drosophila</i>

Mašek, Pavel; Reynolds, Lauren A.; Bollinger, Wesley L.; Moody, Catriona; Mehta, Akshay; Murakami, Kazuma; Yoshizawa, Masato; Gibbs, Allen G.; Keene, Alex C.

doi:10.1242/jeb.103309

Cited by 64 publications

(91 citation statements)

References 59 publications

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“…Drosophila sleep is modulated by external signals (e.g., light and temperature) and internal signals (e.g., circadian clock, sleep pressure, and hunger)163738. Since the induction of arousal is determined by the balance between external and internal impacts, neural mechanisms, which positively and negatively regulate arousal level, are required for keeping the suitable quality and/or quantity of sleep/wake behaviors.…”

Section: Discussionmentioning

confidence: 99%

Modulation of light-driven arousal by LIM-homeodomain transcription factor Apterous in large PDF-positive lateral neurons of the Drosophila brain

Shimada

Inami

Sato

et al. 2016

Sci Rep

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Apterous (Ap), the best studied LIM-homeodomain transcription factor in Drosophila, cooperates with the cofactor Chip (Chi) to regulate transcription of specific target genes. Although Ap regulates various developmental processes, its function in the adult brain remains unclear. Here, we report that Ap and Chi in the neurons expressing PDF, a neuropeptide, play important roles in proper sleep/wake regulation in adult flies. PDF-expressing neurons consist of two neuronal clusters: small ventral-lateral neurons (s-LNvs) acting as the circadian pacemaker and large ventral-lateral neurons (l-LNvs) regulating light-driven arousal. We identified that Ap localizes to the nuclei of s-LNvs and l-LNvs. In light-dark (LD) cycles, RNAi knockdown or the targeted expression of dominant-negative forms of Ap or Chi in PDF-expressing neurons or l-LNvs promoted arousal. In contrast, in constant darkness, knockdown of Ap in PDF-expressing neurons did not promote arousal, indicating that a reduced Ap function in PDF-expressing neurons promotes light-driven arousal. Furthermore, Ap expression in l-LNvs showed daily rhythms (peaking at midnight), which are generated by a direct light-dependent mechanism rather than by the endogenous clock. These results raise the possibility that the daily oscillation of Ap expression in l-LNvs may contribute to the buffering of light-driven arousal in wild-type flies.

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Section: Discussionmentioning

confidence: 99%

Modulation of light-driven arousal by LIM-homeodomain transcription factor Apterous in large PDF-positive lateral neurons of the Drosophila brain

Shimada

Inami

Sato

et al. 2016

Sci Rep

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“…Quantitative genetic approaches in fully sequenced lines have provided insight into the genetic basis for resistance to environmental and physiological stressors including starvation resistance, and identified novel regulators of sleep (Harbison, Yamamoto, Fanara, Norga, & Mackay, ; Vieira et al., ). Further, experimental evolution and artificial selection approaches have revealed a relationship between sleep, feeding, and starvation resistance (Masek et al., ; Slocumb et al., ). For example, 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., ; Seugnet et al., ).…”

Section: Introductionmentioning

confidence: 99%

Variation in sleep and metabolic function is associated with latitude and average temperature in Drosophila melanogaster

Brown

Torres

Bennick

et al. 2018

Ecology and Evolution

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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.

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“…However, unlike larvae, adult flies are intermittent eaters and their foraging behaviors are expected to be much more complex (Masek et al 2014; Qi et al 2015). Compared with larvae, adult flies forage in higher dimensional space and have access to more diverse arrays of food.…”

Section: Introductionmentioning

confidence: 99%

Genetic Architecture of Natural Variation Underlying Adult Foraging Behavior That Is Essential for Survival of Drosophila melanogaster

Ycg

Yang

et al. 2017

Genome Biology and Evolution

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Foraging behavior is critical for the fitness of individuals. However, the genetic basis of variation in foraging behavior and the evolutionary forces underlying such natural variation have rarely been investigated. We developed a systematic approach to assay the variation in survival rate in a foraging environment for adult flies derived from a wild Drosophila melanogaster population. Despite being such an essential trait, there is substantial variation of foraging behavior among D. melanogaster strains. Importantly, we provided the first evaluation of the potential caveats of using inbred Drosophila strains to perform genome-wide association studies on life-history traits, and concluded that inbreeding depression is unlikely a major contributor for the observed large variation in adult foraging behavior. We found that adult foraging behavior has a strong genetic component and, unlike larval foraging behavior, depends on multiple loci. Identified candidate genes are enriched in those with high expression in adult heads and, demonstrated by expression knock down assay, are involved in maintaining normal functions of the nervous system. Our study not only identified candidate genes for foraging behavior that is relevant to individual fitness, but also shed light on the initial stage underlying the evolution of the behavior.

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Altered regulation of sleep and feeding contribute to starvation resistance in Drosophila

Cited by 64 publications

References 59 publications

Modulation of light-driven arousal by LIM-homeodomain transcription factor Apterous in large PDF-positive lateral neurons of the Drosophila brain

Modulation of light-driven arousal by LIM-homeodomain transcription factor Apterous in large PDF-positive lateral neurons of the Drosophila brain

Variation in sleep and metabolic function is associated with latitude and average temperature in Drosophila melanogaster

Genetic Architecture of Natural Variation Underlying Adult Foraging Behavior That Is Essential for Survival of Drosophila melanogaster

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