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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

Selection for DR does not alter sleep.A) Sleep profiles depicting hourly sleep reveal that sleep in SRc flies is increased during both day and night compared to the DRc flies and respective controls (N = 64 for all groups). B) The total sleep duration over 24hrs on food is significantly longer in SRc flies than in FSRc flies. No differences are observed between DRc flies and FDRc flies (SRc group: P<0.001; DRc lines: P>0.05; See S1 Table). C) Beam crossings per waking minute are reduced in DRc and SRc flies compared to respective controls (SRc group: P<0.001; DRc lines: P<0.001; See S1 Table).
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pone.0131275.g003: Selection for DR does not alter sleep.A) Sleep profiles depicting hourly sleep reveal that sleep in SRc flies is increased during both day and night compared to the DRc flies and respective controls (N = 64 for all groups). B) The total sleep duration over 24hrs on food is significantly longer in SRc flies than in FSRc flies. No differences are observed between DRc flies and FDRc flies (SRc group: P<0.001; DRc lines: P>0.05; See S1 Table). C) Beam crossings per waking minute are reduced in DRc and SRc flies compared to respective controls (SRc group: P<0.001; DRc lines: P<0.001; See S1 Table).

Mentions: SR flies sleep longer than their controls, raising the possibility that prolonged sleep is adaptive for survival under conditions of chronic nutrient deprivation [24]. It is possible that the evolution of prolonged sleep either occurs specifically under conditions of starvation, or is a general response to nutrient deprivation. To differentiate between these two possibilities we measured sleep in flies selected for desiccation resistance. There was no difference in the sleep duration between DR and FDR flies (Fig 3 and S3 Fig). In agreement with previous findings, all three SR lines slept longer than FSR controls, but no DR line slept longer than its respective FDR control. This confirms that evolutionary selection for SR, but not DR, results in prolonged sleep (Fig 3 and S3 Fig). Sleep can be differentiated from lethargy or hyperactivity by measuring the amount of activity exhibited when an animal is awake [26]. We measured beam crossings per waking minute to infer waking activity in DR flies to determine if they conserve energy by reducing activity, rather than by extending sleep. Waking activity was reduced in all three DR lines compared to FDR controls, while waking activity was not changed (Group A and B) or reduced (Group C) in SR files (Fig 3C and S3 Fig). Therefore, selection for DR does not result in prolonged sleep, but does reduce activity, providing evidence for distinct energy conservation strategies in response to starvation or desiccation conditions.


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)

Selection for DR does not alter sleep.A) Sleep profiles depicting hourly sleep reveal that sleep in SRc flies is increased during both day and night compared to the DRc flies and respective controls (N = 64 for all groups). B) The total sleep duration over 24hrs on food is significantly longer in SRc flies than in FSRc flies. No differences are observed between DRc flies and FDRc flies (SRc group: P<0.001; DRc lines: P>0.05; See S1 Table). C) Beam crossings per waking minute are reduced in DRc and SRc flies compared to respective controls (SRc group: P<0.001; DRc lines: P<0.001; See S1 Table).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0131275.g003: Selection for DR does not alter sleep.A) Sleep profiles depicting hourly sleep reveal that sleep in SRc flies is increased during both day and night compared to the DRc flies and respective controls (N = 64 for all groups). B) The total sleep duration over 24hrs on food is significantly longer in SRc flies than in FSRc flies. No differences are observed between DRc flies and FDRc flies (SRc group: P<0.001; DRc lines: P>0.05; See S1 Table). C) Beam crossings per waking minute are reduced in DRc and SRc flies compared to respective controls (SRc group: P<0.001; DRc lines: P<0.001; See S1 Table).
Mentions: SR flies sleep longer than their controls, raising the possibility that prolonged sleep is adaptive for survival under conditions of chronic nutrient deprivation [24]. It is possible that the evolution of prolonged sleep either occurs specifically under conditions of starvation, or is a general response to nutrient deprivation. To differentiate between these two possibilities we measured sleep in flies selected for desiccation resistance. There was no difference in the sleep duration between DR and FDR flies (Fig 3 and S3 Fig). In agreement with previous findings, all three SR lines slept longer than FSR controls, but no DR line slept longer than its respective FDR control. This confirms that evolutionary selection for SR, but not DR, results in prolonged sleep (Fig 3 and S3 Fig). Sleep can be differentiated from lethargy or hyperactivity by measuring the amount of activity exhibited when an animal is awake [26]. We measured beam crossings per waking minute to infer waking activity in DR flies to determine if they conserve energy by reducing activity, rather than by extending sleep. Waking activity was reduced in all three DR lines compared to FDR controls, while waking activity was not changed (Group A and B) or reduced (Group C) in SR files (Fig 3C and S3 Fig). Therefore, selection for DR does not result in prolonged sleep, but does reduce activity, providing evidence for distinct energy conservation strategies in response to starvation or desiccation conditions.

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