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

Slocumb ME, Regalado JM, Yoshizawa M, Neely GG, Masek P, Gibbs AG, Keene AC - PLoS ONE (2015)

Bottom Line: 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.Thermotolerance is not altered in starvation or desiccation resistant flies, providing further evidence for context-specific adaptation to environmental stressors.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Nevada-Reno, Reno, NV, 89557, United States of America.

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.

No MeSH data available.


Related in: MedlinePlus

Sleep enhances starvation resistance in SR-DR hybrid flies.A) Schematic of behavioral analysis. F2 progeny were generated by crossing SR and DR parental lines. Individuals were then tested for sleep on food over 24hrs, followed by longevity under starvation or desiccation conditions. B) Correlation analysis for SRc-DRc F2 hybrids reveals a correlation between sleep duration on food and starvation resistance (N = 32 for starved; P<0.01; R2 = 0.482). C) No correlation is observed between desiccation resistance and sleep duration on food in SRc-DRc F2 hybrid flies (N = 30 for desiccated; P>0.05; R2 = 0.01). D, E) No correlation between sleep duration and longevity was observed in flies from SRa-DRa crosses for either starvation or desiccation (N = 32; P>0.05; R2 = 0.043; N = 32; P>0.05; R2 = 0.006). F, G) Sleep duration was correlated with starvation resistance in SRb-DRb F2 hybrid flies (N = 31; P<0.05; R2 = 0.289), while no correlation was observed between sleep duration and desiccation resistance (N = 32; P>0.05; R2 = 0.068).
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pone.0131275.g005: Sleep enhances starvation resistance in SR-DR hybrid flies.A) Schematic of behavioral analysis. F2 progeny were generated by crossing SR and DR parental lines. Individuals were then tested for sleep on food over 24hrs, followed by longevity under starvation or desiccation conditions. B) Correlation analysis for SRc-DRc F2 hybrids reveals a correlation between sleep duration on food and starvation resistance (N = 32 for starved; P<0.01; R2 = 0.482). C) No correlation is observed between desiccation resistance and sleep duration on food in SRc-DRc F2 hybrid flies (N = 30 for desiccated; P>0.05; R2 = 0.01). D, E) No correlation between sleep duration and longevity was observed in flies from SRa-DRa crosses for either starvation or desiccation (N = 32; P>0.05; R2 = 0.043; N = 32; P>0.05; R2 = 0.006). F, G) Sleep duration was correlated with starvation resistance in SRb-DRb F2 hybrid flies (N = 31; P<0.05; R2 = 0.289), while no correlation was observed between sleep duration and desiccation resistance (N = 32; P>0.05; R2 = 0.068).

Mentions: The enhanced sleep duration of SR flies raises the possibility that extended sleep is advantageous under conditions of chronic starvation, but not desiccation. To directly test this hypothesis we generated F2 hybrids between SR and DR flies. Individual F2 flies were tested for sleep duration on food, then transferred to starvation or desiccation conditions, and the relationship between sleep on food and resistance to nutrient deprivation was determined (Fig 5A). A significant positive correlation between sleep and starvation resistance was observed between SRb-DRb and SRc-DRc populations, suggesting that prolonged sleep is adaptive in food-deprived conditions (Fig 5B and 5F). However, there was no correlation in SRa-DRa hybrids, raising the possibility that the advantageous effects of sleep in response to starvation are more dependent on genetic background and evolutionary history (Fig 5D). No relationship was observed between sleep and desiccation resistance for any of the pairings tested (Fig 5C, 5E and 5G). Therefore, prolonged sleep appears to explain up to 30% of the resistance to starvation. Taken together with the prolonged sleep of SR flies, these findings support the notion that adaptations in response to starvation and desiccation conditions result in distinct behavioral and physiological alterations.


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

Slocumb ME, Regalado JM, Yoshizawa M, Neely GG, Masek P, Gibbs AG, Keene AC - PLoS ONE (2015)

Sleep enhances starvation resistance in SR-DR hybrid flies.A) Schematic of behavioral analysis. F2 progeny were generated by crossing SR and DR parental lines. Individuals were then tested for sleep on food over 24hrs, followed by longevity under starvation or desiccation conditions. B) Correlation analysis for SRc-DRc F2 hybrids reveals a correlation between sleep duration on food and starvation resistance (N = 32 for starved; P<0.01; R2 = 0.482). C) No correlation is observed between desiccation resistance and sleep duration on food in SRc-DRc F2 hybrid flies (N = 30 for desiccated; P>0.05; R2 = 0.01). D, E) No correlation between sleep duration and longevity was observed in flies from SRa-DRa crosses for either starvation or desiccation (N = 32; P>0.05; R2 = 0.043; N = 32; P>0.05; R2 = 0.006). F, G) Sleep duration was correlated with starvation resistance in SRb-DRb F2 hybrid flies (N = 31; P<0.05; R2 = 0.289), while no correlation was observed between sleep duration and desiccation resistance (N = 32; P>0.05; R2 = 0.068).
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pone.0131275.g005: Sleep enhances starvation resistance in SR-DR hybrid flies.A) Schematic of behavioral analysis. F2 progeny were generated by crossing SR and DR parental lines. Individuals were then tested for sleep on food over 24hrs, followed by longevity under starvation or desiccation conditions. B) Correlation analysis for SRc-DRc F2 hybrids reveals a correlation between sleep duration on food and starvation resistance (N = 32 for starved; P<0.01; R2 = 0.482). C) No correlation is observed between desiccation resistance and sleep duration on food in SRc-DRc F2 hybrid flies (N = 30 for desiccated; P>0.05; R2 = 0.01). D, E) No correlation between sleep duration and longevity was observed in flies from SRa-DRa crosses for either starvation or desiccation (N = 32; P>0.05; R2 = 0.043; N = 32; P>0.05; R2 = 0.006). F, G) Sleep duration was correlated with starvation resistance in SRb-DRb F2 hybrid flies (N = 31; P<0.05; R2 = 0.289), while no correlation was observed between sleep duration and desiccation resistance (N = 32; P>0.05; R2 = 0.068).
Mentions: The enhanced sleep duration of SR flies raises the possibility that extended sleep is advantageous under conditions of chronic starvation, but not desiccation. To directly test this hypothesis we generated F2 hybrids between SR and DR flies. Individual F2 flies were tested for sleep duration on food, then transferred to starvation or desiccation conditions, and the relationship between sleep on food and resistance to nutrient deprivation was determined (Fig 5A). A significant positive correlation between sleep and starvation resistance was observed between SRb-DRb and SRc-DRc populations, suggesting that prolonged sleep is adaptive in food-deprived conditions (Fig 5B and 5F). However, there was no correlation in SRa-DRa hybrids, raising the possibility that the advantageous effects of sleep in response to starvation are more dependent on genetic background and evolutionary history (Fig 5D). No relationship was observed between sleep and desiccation resistance for any of the pairings tested (Fig 5C, 5E and 5G). Therefore, prolonged sleep appears to explain up to 30% of the resistance to starvation. Taken together with the prolonged sleep of SR flies, these findings support the notion that adaptations in response to starvation and desiccation conditions result in distinct behavioral and physiological alterations.

Bottom Line: 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.Thermotolerance is not altered in starvation or desiccation resistant flies, providing further evidence for context-specific adaptation to environmental stressors.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Nevada-Reno, Reno, NV, 89557, United States of America.

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.

No MeSH data available.


Related in: MedlinePlus