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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

Distinct resistance to nutrient deprivation in SR and DR flies.Survival of flies placed in activity monitors under starvation conditions. A) Flies from the SRc lines survived longer than FSRc controls, whereas DR lines do not differ from FDRc controls (SR lines: P < 0.001 in all groups; DR lines: P>0.05). B) DRc flies survive longer than FDRc controls under desiccation conditions. SRc flies were also resistant to desiccation compared to FSRc controls (DRc line: P<0.001; SRc line: P<0.001, See S1 Table.) C) SRc flies did not live as long as FSRc controls, and no difference in longevity was observed in DRc flies and controls, under thermal stress conditions (SR lines: P = 0.01; DR lines P>0.05; See S1 Table).
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pone.0131275.g002: Distinct resistance to nutrient deprivation in SR and DR flies.Survival of flies placed in activity monitors under starvation conditions. A) Flies from the SRc lines survived longer than FSRc controls, whereas DR lines do not differ from FDRc controls (SR lines: P < 0.001 in all groups; DR lines: P>0.05). B) DRc flies survive longer than FDRc controls under desiccation conditions. SRc flies were also resistant to desiccation compared to FSRc controls (DRc line: P<0.001; SRc line: P<0.001, See S1 Table.) C) SRc flies did not live as long as FSRc controls, and no difference in longevity was observed in DRc flies and controls, under thermal stress conditions (SR lines: P = 0.01; DR lines P>0.05; See S1 Table).

Mentions: To determine whether each selection protocols generally enhanced stress resistance or increased survival to nutrient deprivation in a context-dependent fashion we measured longevity of SR and DR selected flies under starvation and desiccation conditions. Following 24hrs of acclimation on food, flies were transferred to tubes containing 1% agar or dry Kimwipes. Survival time was measured using the Drosophila Activity Monitor (DAM) system [29]. Under starvation conditions, all three SR groups survived longer than FSR and FDR controls and DR flies (Fig 2A and S2 Fig). However, two groups of desiccation selected DR flies survived longer than associated controls, suggesting that selection for desiccation resistance may confer moderate starvation resistance (Fig 2A and S2 Fig). Under desiccation conditions, all three groups of SR flies survived longer than FSR group controls, and all three groups of desiccation selected DR flies survived longer than FDR controls (Fig 2B and S2 Fig). Therefore, experimental selection for starvation or desiccation resistance has differential effects on the evolution of resistance to nutrient deprivation.


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)

Distinct resistance to nutrient deprivation in SR and DR flies.Survival of flies placed in activity monitors under starvation conditions. A) Flies from the SRc lines survived longer than FSRc controls, whereas DR lines do not differ from FDRc controls (SR lines: P < 0.001 in all groups; DR lines: P>0.05). B) DRc flies survive longer than FDRc controls under desiccation conditions. SRc flies were also resistant to desiccation compared to FSRc controls (DRc line: P<0.001; SRc line: P<0.001, See S1 Table.) C) SRc flies did not live as long as FSRc controls, and no difference in longevity was observed in DRc flies and controls, under thermal stress conditions (SR lines: P = 0.01; DR lines P>0.05; See S1 Table).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4493134&req=5

pone.0131275.g002: Distinct resistance to nutrient deprivation in SR and DR flies.Survival of flies placed in activity monitors under starvation conditions. A) Flies from the SRc lines survived longer than FSRc controls, whereas DR lines do not differ from FDRc controls (SR lines: P < 0.001 in all groups; DR lines: P>0.05). B) DRc flies survive longer than FDRc controls under desiccation conditions. SRc flies were also resistant to desiccation compared to FSRc controls (DRc line: P<0.001; SRc line: P<0.001, See S1 Table.) C) SRc flies did not live as long as FSRc controls, and no difference in longevity was observed in DRc flies and controls, under thermal stress conditions (SR lines: P = 0.01; DR lines P>0.05; See S1 Table).
Mentions: To determine whether each selection protocols generally enhanced stress resistance or increased survival to nutrient deprivation in a context-dependent fashion we measured longevity of SR and DR selected flies under starvation and desiccation conditions. Following 24hrs of acclimation on food, flies were transferred to tubes containing 1% agar or dry Kimwipes. Survival time was measured using the Drosophila Activity Monitor (DAM) system [29]. Under starvation conditions, all three SR groups survived longer than FSR and FDR controls and DR flies (Fig 2A and S2 Fig). However, two groups of desiccation selected DR flies survived longer than associated controls, suggesting that selection for desiccation resistance may confer moderate starvation resistance (Fig 2A and S2 Fig). Under desiccation conditions, all three groups of SR flies survived longer than FSR group controls, and all three groups of desiccation selected DR flies survived longer than FDR controls (Fig 2B and S2 Fig). Therefore, experimental selection for starvation or desiccation resistance has differential effects on the evolution of resistance to nutrient deprivation.

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