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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

Resistance to nutrient deprivation in DR is not confounded by starvation during selection.A) Schematic of selection process for yoked-control flies (DRCTRLa and DRCTRLb) that were starved during the selection period for DR flies. Of the three groups originally generated, only two remain. B, C) Survival of DRCTRLa and DRCTRLb flies does not differ from respective FDR controls under starvation conditions. D, E) Survival of DRCTRLa and DRCTRLb flies does not differ from respective FDR controls under desiccation conditions. F, G) Sleep is not increased in the DRCTRLa and DRCTRLb flies compared to their respective FDR controls or DR selected experimental groups. Sleep is significantly less than respective SR selected flies. H) Beam crossings per waking minute, an meausre of activity while awake, were reduced in DRCTRLa flies compared to FDRa controls, and was significantly greater than SRa selected flies. I) Beam crossings per waking minute did not differ between DRCTRLb and FDRb flies and was significantly greater than both DRb and SRb selected lines. *** denotes P<0.001.
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pone.0131275.g004: Resistance to nutrient deprivation in DR is not confounded by starvation during selection.A) Schematic of selection process for yoked-control flies (DRCTRLa and DRCTRLb) that were starved during the selection period for DR flies. Of the three groups originally generated, only two remain. B, C) Survival of DRCTRLa and DRCTRLb flies does not differ from respective FDR controls under starvation conditions. D, E) Survival of DRCTRLa and DRCTRLb flies does not differ from respective FDR controls under desiccation conditions. F, G) Sleep is not increased in the DRCTRLa and DRCTRLb flies compared to their respective FDR controls or DR selected experimental groups. Sleep is significantly less than respective SR selected flies. H) Beam crossings per waking minute, an meausre of activity while awake, were reduced in DRCTRLa flies compared to FDRa controls, and was significantly greater than SRa selected flies. I) Beam crossings per waking minute did not differ between DRCTRLb and FDRb flies and was significantly greater than both DRb and SRb selected lines. *** denotes P<0.001.

Mentions: The selection protocol used to generate DR flies creates a state of both food and water deprivation, raising the possibility that resistance to nutrient deprivation and the altered activity levels of DR flies are due to starvation. To account for this possibility we assayed yoked-control flies (DRCTRL) that were starved for the period that DR flies were desiccated throughout DR selection (Fig 4A). Only two of the three originally selected DRCTRL groups remain. Survival under starvation conditions (Fig 4B and 4C) and desiccation conditions (Fig 4D and 4E) did not differ between DRCTRL flies or FDR control flies, suggesting that the resistance to nutrient deprivation observed in DR flies results from desiccation selection specifically. Flies from the SRa and SRb groups survived significantly longer than their FDR and DRCTRL controls. This indicates that the relatively short starvation selection time used for DR selection (~3–4 days) is insufficient to confer changes in starvation resistance (Fig 4B and 4C). Further, DRa and DRb group flies survived longer under desiccation conditions than their DRCTRL flies, confirming that survival under desiccation conditions in DR flies is not due to starvation during the selection procedure.


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)

Resistance to nutrient deprivation in DR is not confounded by starvation during selection.A) Schematic of selection process for yoked-control flies (DRCTRLa and DRCTRLb) that were starved during the selection period for DR flies. Of the three groups originally generated, only two remain. B, C) Survival of DRCTRLa and DRCTRLb flies does not differ from respective FDR controls under starvation conditions. D, E) Survival of DRCTRLa and DRCTRLb flies does not differ from respective FDR controls under desiccation conditions. F, G) Sleep is not increased in the DRCTRLa and DRCTRLb flies compared to their respective FDR controls or DR selected experimental groups. Sleep is significantly less than respective SR selected flies. H) Beam crossings per waking minute, an meausre of activity while awake, were reduced in DRCTRLa flies compared to FDRa controls, and was significantly greater than SRa selected flies. I) Beam crossings per waking minute did not differ between DRCTRLb and FDRb flies and was significantly greater than both DRb and SRb selected lines. *** denotes P<0.001.
© Copyright Policy
Related In: Results  -  Collection

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

pone.0131275.g004: Resistance to nutrient deprivation in DR is not confounded by starvation during selection.A) Schematic of selection process for yoked-control flies (DRCTRLa and DRCTRLb) that were starved during the selection period for DR flies. Of the three groups originally generated, only two remain. B, C) Survival of DRCTRLa and DRCTRLb flies does not differ from respective FDR controls under starvation conditions. D, E) Survival of DRCTRLa and DRCTRLb flies does not differ from respective FDR controls under desiccation conditions. F, G) Sleep is not increased in the DRCTRLa and DRCTRLb flies compared to their respective FDR controls or DR selected experimental groups. Sleep is significantly less than respective SR selected flies. H) Beam crossings per waking minute, an meausre of activity while awake, were reduced in DRCTRLa flies compared to FDRa controls, and was significantly greater than SRa selected flies. I) Beam crossings per waking minute did not differ between DRCTRLb and FDRb flies and was significantly greater than both DRb and SRb selected lines. *** denotes P<0.001.
Mentions: The selection protocol used to generate DR flies creates a state of both food and water deprivation, raising the possibility that resistance to nutrient deprivation and the altered activity levels of DR flies are due to starvation. To account for this possibility we assayed yoked-control flies (DRCTRL) that were starved for the period that DR flies were desiccated throughout DR selection (Fig 4A). Only two of the three originally selected DRCTRL groups remain. Survival under starvation conditions (Fig 4B and 4C) and desiccation conditions (Fig 4D and 4E) did not differ between DRCTRL flies or FDR control flies, suggesting that the resistance to nutrient deprivation observed in DR flies results from desiccation selection specifically. Flies from the SRa and SRb groups survived significantly longer than their FDR and DRCTRL controls. This indicates that the relatively short starvation selection time used for DR selection (~3–4 days) is insufficient to confer changes in starvation resistance (Fig 4B and 4C). Further, DRa and DRb group flies survived longer under desiccation conditions than their DRCTRL flies, confirming that survival under desiccation conditions in DR flies is not due to starvation during the selection procedure.

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