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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

SR and DR selection increases body size and alters metabolic profile.A) Schematic of selection processes for SR and DR flies. Adult outbred flies were placed under desiccation or starvation conditions until ~15% of the flies survived. The flies were then moved to food. This process was repeated over >80 generations. The FDR controls were placed on agar during desiccation selection to account for food deprivation in DR selected flies. There were three replicated SR populations (designated SRa, SRb and SRc) and three fed control populations (FSRa, FSRb and FSRc). For DR experiments there were three replicated groups (designated DRa, DRb and DRc) and three fed control populations (FDRa, FDRb and FDRc). B) Flies from the C Group. SRc and DRc flies are visibly larger than FSRc and FDRc controls. C) Triglyceride levels are elevated in the SRc flies compared to FSRc controls. No differences are observed between DRc flies and FDRc controls (P<0.001; See S1 Table). D) Glycogen levels were greater in DRc flies than in FDRc controls. No differences were present between SRc flies and FSRc controls (P<0.001; See S1 Table). E) Free glucose levels did not differ between SRc or DRc flies and their respective controls (P>0.05; See S1 Table).
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pone.0131275.g001: SR and DR selection increases body size and alters metabolic profile.A) Schematic of selection processes for SR and DR flies. Adult outbred flies were placed under desiccation or starvation conditions until ~15% of the flies survived. The flies were then moved to food. This process was repeated over >80 generations. The FDR controls were placed on agar during desiccation selection to account for food deprivation in DR selected flies. There were three replicated SR populations (designated SRa, SRb and SRc) and three fed control populations (FSRa, FSRb and FSRc). For DR experiments there were three replicated groups (designated DRa, DRb and DRc) and three fed control populations (FDRa, FDRb and FDRc). B) Flies from the C Group. SRc and DRc flies are visibly larger than FSRc and FDRc controls. C) Triglyceride levels are elevated in the SRc flies compared to FSRc controls. No differences are observed between DRc flies and FDRc controls (P<0.001; See S1 Table). D) Glycogen levels were greater in DRc flies than in FDRc controls. No differences were present between SRc flies and FSRc controls (P<0.001; See S1 Table). E) Free glucose levels did not differ between SRc or DRc flies and their respective controls (P>0.05; See S1 Table).

Mentions: The wild-derived stocks used in this study were collected with owner’s permission from Terhune Orchards in Princeton, N.J. in 1999 and have been maintained as outbred stocks at 25°C on standard corn meal medium since this time. The generation of DR and fed control FDR flies have previously been described as Td and Tf flies, respectively ([23] and Fig 1B). These have been renamed in this manuscript for clarity, with the three replicated DR populations being designated as DRa, DRb, and DRc, and the three fed control populations as FDRa, FDRb, and FDRc. Briefly, these three populations of DR flies were selected from the founding stock that had been maintained on standard food conditions. Selection for desiccation resistance in DR flies occurred by transferring populations of ~7,500 adult flies to a population cage containing silica gel desiccant alone. The silica gel was replaced with fly food when ~15% of the flies survived. Eggs were then collected from the progeny, and this cycle was repeated for 30 generations to develop the previously described DR lines. The DR lines used in this paper have been maintained under reduced desiccation selection (24 hours under desiccation for each generation) for ~110 generations. The FDR flies used in this paper were three replicate fed control populations maintained on food throughout the selection process (Fig 1B). Because desiccation selection involves removal of both food and water, an additional population of lines was generated where food deprivation was yoked to the desiccation selected Drosophila. These flies were provided agar instead of the silica gel desiccant, and flies were transferred at the same times as DR group flies [23]. Of the three groups originally generated, only two remain, and these flies have been renamed DRCTRLa and DRCTRLb for clarity.


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)

SR and DR selection increases body size and alters metabolic profile.A) Schematic of selection processes for SR and DR flies. Adult outbred flies were placed under desiccation or starvation conditions until ~15% of the flies survived. The flies were then moved to food. This process was repeated over >80 generations. The FDR controls were placed on agar during desiccation selection to account for food deprivation in DR selected flies. There were three replicated SR populations (designated SRa, SRb and SRc) and three fed control populations (FSRa, FSRb and FSRc). For DR experiments there were three replicated groups (designated DRa, DRb and DRc) and three fed control populations (FDRa, FDRb and FDRc). B) Flies from the C Group. SRc and DRc flies are visibly larger than FSRc and FDRc controls. C) Triglyceride levels are elevated in the SRc flies compared to FSRc controls. No differences are observed between DRc flies and FDRc controls (P<0.001; See S1 Table). D) Glycogen levels were greater in DRc flies than in FDRc controls. No differences were present between SRc flies and FSRc controls (P<0.001; See S1 Table). E) Free glucose levels did not differ between SRc or DRc flies and their respective controls (P>0.05; See S1 Table).
© Copyright Policy
Related In: Results  -  Collection

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

pone.0131275.g001: SR and DR selection increases body size and alters metabolic profile.A) Schematic of selection processes for SR and DR flies. Adult outbred flies were placed under desiccation or starvation conditions until ~15% of the flies survived. The flies were then moved to food. This process was repeated over >80 generations. The FDR controls were placed on agar during desiccation selection to account for food deprivation in DR selected flies. There were three replicated SR populations (designated SRa, SRb and SRc) and three fed control populations (FSRa, FSRb and FSRc). For DR experiments there were three replicated groups (designated DRa, DRb and DRc) and three fed control populations (FDRa, FDRb and FDRc). B) Flies from the C Group. SRc and DRc flies are visibly larger than FSRc and FDRc controls. C) Triglyceride levels are elevated in the SRc flies compared to FSRc controls. No differences are observed between DRc flies and FDRc controls (P<0.001; See S1 Table). D) Glycogen levels were greater in DRc flies than in FDRc controls. No differences were present between SRc flies and FSRc controls (P<0.001; See S1 Table). E) Free glucose levels did not differ between SRc or DRc flies and their respective controls (P>0.05; See S1 Table).
Mentions: The wild-derived stocks used in this study were collected with owner’s permission from Terhune Orchards in Princeton, N.J. in 1999 and have been maintained as outbred stocks at 25°C on standard corn meal medium since this time. The generation of DR and fed control FDR flies have previously been described as Td and Tf flies, respectively ([23] and Fig 1B). These have been renamed in this manuscript for clarity, with the three replicated DR populations being designated as DRa, DRb, and DRc, and the three fed control populations as FDRa, FDRb, and FDRc. Briefly, these three populations of DR flies were selected from the founding stock that had been maintained on standard food conditions. Selection for desiccation resistance in DR flies occurred by transferring populations of ~7,500 adult flies to a population cage containing silica gel desiccant alone. The silica gel was replaced with fly food when ~15% of the flies survived. Eggs were then collected from the progeny, and this cycle was repeated for 30 generations to develop the previously described DR lines. The DR lines used in this paper have been maintained under reduced desiccation selection (24 hours under desiccation for each generation) for ~110 generations. The FDR flies used in this paper were three replicate fed control populations maintained on food throughout the selection process (Fig 1B). Because desiccation selection involves removal of both food and water, an additional population of lines was generated where food deprivation was yoked to the desiccation selected Drosophila. These flies were provided agar instead of the silica gel desiccant, and flies were transferred at the same times as DR group flies [23]. Of the three groups originally generated, only two remain, and these flies have been renamed DRCTRLa and DRCTRLb for clarity.

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