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Enhanced Sleep Is an Evolutionarily Adaptive Response to Starvation Stress in Drosophila

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...

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Autores principales: Slocumb, Melissa E., Regalado, Josue M., Yoshizawa, Masato, Neely, Greg G., Masek, Pavel, Gibbs, Allen G., Keene, Alex C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4493134/
https://www.ncbi.nlm.nih.gov/pubmed/26147198
http://dx.doi.org/10.1371/journal.pone.0131275
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author Slocumb, Melissa E.
Regalado, Josue M.
Yoshizawa, Masato
Neely, Greg G.
Masek, Pavel
Gibbs, Allen G.
Keene, Alex C.
author_facet Slocumb, Melissa E.
Regalado, Josue M.
Yoshizawa, Masato
Neely, Greg G.
Masek, Pavel
Gibbs, Allen G.
Keene, Alex C.
author_sort Slocumb, Melissa E.
collection PubMed
description 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. F(2) 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.
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spelling pubmed-44931342015-07-15 Enhanced Sleep Is an Evolutionarily Adaptive Response to Starvation Stress in Drosophila Slocumb, Melissa E. Regalado, Josue M. Yoshizawa, Masato Neely, Greg G. Masek, Pavel Gibbs, Allen G. Keene, Alex C. PLoS One Research Article 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. F(2) 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. Public Library of Science 2015-07-06 /pmc/articles/PMC4493134/ /pubmed/26147198 http://dx.doi.org/10.1371/journal.pone.0131275 Text en © 2015 Slocumb et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Slocumb, Melissa E.
Regalado, Josue M.
Yoshizawa, Masato
Neely, Greg G.
Masek, Pavel
Gibbs, Allen G.
Keene, Alex C.
Enhanced Sleep Is an Evolutionarily Adaptive Response to Starvation Stress in Drosophila
title Enhanced Sleep Is an Evolutionarily Adaptive Response to Starvation Stress in Drosophila
title_full Enhanced Sleep Is an Evolutionarily Adaptive Response to Starvation Stress in Drosophila
title_fullStr Enhanced Sleep Is an Evolutionarily Adaptive Response to Starvation Stress in Drosophila
title_full_unstemmed Enhanced Sleep Is an Evolutionarily Adaptive Response to Starvation Stress in Drosophila
title_short Enhanced Sleep Is an Evolutionarily Adaptive Response to Starvation Stress in Drosophila
title_sort enhanced sleep is an evolutionarily adaptive response to starvation stress in drosophila
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4493134/
https://www.ncbi.nlm.nih.gov/pubmed/26147198
http://dx.doi.org/10.1371/journal.pone.0131275
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