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• W2893389670 abstract "•Fruit flies switch their feeding preference from yeast to plants at low temperature•Flies need PUFAs from plants to increase membrane lipid unsaturation in the cold•Dietary plant lipids maintain membrane fluidity and improve survival in the cold How cold-blooded animals acclimate to temperature and what determines the limits of their viable temperature range are not understood. Here, we show that Drosophila alter their dietary preference from yeast to plants when temperatures drop below 15°C and that the different lipids present in plants improve survival at low temperatures. We show that Drosophila require dietary unsaturated fatty acids present in plants to adjust membrane fluidity and maintain motor coordination. Feeding on plants extends lifespan and survival for many months at temperatures consistent with overwintering in temperate climates. Thus, physiological alterations caused by a temperature-dependent dietary shift could help Drosophila survive seasonal temperature changes. How cold-blooded animals acclimate to temperature and what determines the limits of their viable temperature range are not understood. Here, we show that Drosophila alter their dietary preference from yeast to plants when temperatures drop below 15°C and that the different lipids present in plants improve survival at low temperatures. We show that Drosophila require dietary unsaturated fatty acids present in plants to adjust membrane fluidity and maintain motor coordination. Feeding on plants extends lifespan and survival for many months at temperatures consistent with overwintering in temperate climates. Thus, physiological alterations caused by a temperature-dependent dietary shift could help Drosophila survive seasonal temperature changes. Cold-blooded animals develop and reproduce successfully over a wide temperature range. Drosophila melanogaster provides a powerful genetic system in which to probe the mechanisms underlying temperature acclimation. The genetic regulatory networks underlying its growth and metabolism have been well studied, and there has been extensive work on its ecology and population genetics. Populations of Drosophila melanogaster are thought to survive year-round in temperate and tropical climates and are found in habitats with a wide range of average seasonal temperature fluctuations (Hoffmann, 2010Hoffmann A.A. Physiological climatic limits in Drosophila: patterns and implications.J. Exp. Biol. 2010; 213: 870-880Crossref PubMed Scopus (265) Google Scholar). The response of Drosophila adults to temperature extremes has been studied in the lab using Drosophila stocks recently established from wild populations and then maintained on lab diets. While successful development is restricted to the range between 12°C and 30°C, Drosophila can withstand a few hours at higher (38°C) and lower (−2°C) temperature extremes (Hoffmann, 2010Hoffmann A.A. Physiological climatic limits in Drosophila: patterns and implications.J. Exp. Biol. 2010; 213: 870-880Crossref PubMed Scopus (265) Google Scholar, Hoffmann et al., 2002Hoffmann A.A. Anderson A. Hallas R. Opposing clines for high and low temperature resistance in Drosophila melanogaster.Ecol. Lett. 2002; 5: 614-618Crossref Scopus (358) Google Scholar). These limits can vary somewhat depending on the geographical area from which the flies are isolated and can be extended by “hardening,” i.e., pre-exposure to high or low temperatures (Kelty and Lee, 1999Kelty J.D. Lee R.E. Induction of rapid cold hardening by cooling at ecologically relevant rates in Drosophila melanogaster.J. Insect Physiol. 1999; 45: 719-726Crossref PubMed Scopus (178) Google Scholar, Kelty and Lee, 2001Kelty J.D. Lee R.E. Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophiladae) during ecologically based thermoperiodic cycles.J. Exp. Biol. 2001; 204: 1659-1666PubMed Google Scholar, Sejerkilde et al., 2003Sejerkilde M. Sørensen J.G. Loeschcke V. Effects of cold- and heat hardening on thermal resistance in Drosophila melanogaster.J. Insect Physiol. 2003; 49: 719-726Crossref PubMed Scopus (116) Google Scholar). Since temperatures even in temperate climates can exceed these limits, it seems likely that Drosophila must behave in a way that enables them to avoid extreme temperatures in their natural environments, that key ingredients in temperature acclimation are missing from the lab, or both. It is unclear exactly where or how Drosophila melanogaster overwinter in the wild. Seasonal changes in temperature pose interesting challenges for cold-blooded animals because temperature strongly influences the rates of biochemical reactions and the physical properties of matter, such as the phase transition-dependent temporal and spatial organization of the cytoplasm (Banani et al., 2017Banani S.F. Lee H.O. Hyman A.A. Rosen M.K. Biomolecular condensates: organizers of cellular biochemistry.Nat. Rev. Mol. Cell Biol. 2017; 18: 285-298Crossref PubMed Scopus (2254) Google Scholar) and cellular membranes (Sezgin et al., 2017Sezgin E. Levental I. Mayor S. Eggeling C. The mystery of membrane organization: composition, regulation and roles of lipid rafts.Nat. Rev. Mol. Cell Biol. 2017; 18: 361-374Crossref PubMed Scopus (1027) Google Scholar, Veatch et al., 2008Veatch S.L. Cicuta P. Sengupta P. Honerkamp-Smith A. Holowka D. Baird B. Critical fluctuations in plasma membrane vesicles.ACS Chem. Biol. 2008; 3: 287-293Crossref PubMed Scopus (367) Google Scholar). Temperature alters the fluidity, ion permeability, and phase behavior of lipid bilayers (Hazel, 1995Hazel J.R. Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?.Annu. Rev. Physiol. 1995; 57: 19-42Crossref PubMed Scopus (930) Google Scholar), and maintaining membrane biophysical properties within a functional range is essential for life at changing temperature. Phase separation underlies formation of membrane micro-domains involved in protein sorting and signaling (Cebecauer and Holowka, 2017Cebecauer M. Holowka D. Editorial. Molecular organization of membranes: where biology meets biophysics.Front. Cell Dev. Biol. 2017; 5: 113Crossref PubMed Scopus (1) Google Scholar, Lingwood and Simons, 2010Lingwood D. Simons K. Lipid rafts as a membrane-organizing principle.Science. 2010; 327: 46-50Crossref PubMed Scopus (3213) Google Scholar). Furthermore, membrane fluidity can modulate the activity of membrane proteins—for example, the Na+/K+ ATPase, which maintains ion homeostasis and membrane potential (Bhatia et al., 2016Bhatia T. Cornelius F. Brewer J. Bagatolli L.A. Simonsen A.C. Ipsen J.H. Mouritsen O.G. Spatial distribution and activity of Na(+)/K(+)-ATPase in lipid bilayer membranes with phase boundaries.Biochim. Biophys. Acta. 2016; 1858: 1390-1399Crossref PubMed Scopus (26) Google Scholar, Cornelius et al., 2015Cornelius F. Habeck M. Kanai R. Toyoshima C. Karlish S.J. General and specific lipid-protein interactions in Na,K-ATPase.Biochim. Biophys. Acta. 2015; 1848: 1729-1743Crossref PubMed Scopus (102) Google Scholar, Wu et al., 2001Wu B.J. Else P.L. Storlien L.H. Hulbert A.J. Molecular activity of Na(+)/K(+)-ATPase from different sources is related to the packing of membrane lipids.J. Exp. Biol. 2001; 204: 4271-4280PubMed Google Scholar). Excessive rigidity of membranes at low temperatures may account for the loss of K+ homeostasis and membrane potential associated with chill coma in insects (Macmillan and Sinclair, 2011Macmillan H.A. Sinclair B.J. Mechanisms underlying insect chill-coma.J. Insect Physiol. 2011; 57: 12-20Crossref PubMed Scopus (223) Google Scholar). Bacteria, fungi, plants, and some animals have been observed to alter their membrane composition when the temperature changes to at least partially compensate for temperature—a phenomenon known as homeoviscous or homeophasic adaptation (Hazel, 1995Hazel J.R. Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation?.Annu. Rev. Physiol. 1995; 57: 19-42Crossref PubMed Scopus (930) Google Scholar). Decreasing temperature is associated with increasing fatty acid unsaturation, shorter fatty acid chain length, and an elevation in the PE/PC ratio—all of which are predicted to increase membrane fluidity (Cossins et al., 1977Cossins A.R. Friedlander M.J. Prosser C.L. Correlations between behavioral temperature adaptations of goldfish and viscosity and fatty acid composition of their synaptic membranes.J. Comp. Physiol. 1977; 120: 109-121Crossref Scopus (120) Google Scholar, Cossins and Prosser, 1978Cossins A.R. Prosser C.L. Evolutionary adaptation of membranes to temperature.Proc. Natl. Acad. Sci. USA. 1978; 75: 2040-2043Crossref PubMed Scopus (210) Google Scholar, Kemp and Smith, 1970Kemp P. Smith M.W. Effect of temperature acclimatization on the fatty acid composition of goldfish intestinal lipids.Biochem. J. 1970; 117: 9-15Crossref PubMed Scopus (81) Google Scholar). The physiological changes that occur in Drosophila melanogaster during rapid cold hardening and other types of cold exposure have been explored using metabolomics, lipidomics, proteomics, and transcriptomics (Colinet et al., 2013Colinet H. Overgaard J. Com E. Sørensen J.G. Proteomic profiling of thermal acclimation in Drosophila melanogaster.Insect Biochem. Mol. Biol. 2013; 43: 352-365Crossref PubMed Scopus (66) Google Scholar, Koštál et al., 2011Koštál V. Korbelová J. Rozsypal J. Zahradníčková H. Cimlová J. Tomčala A. Šimek P. Long-term cold acclimation extends survival time at 0 degrees C and modifies the metabolomic profiles of the larvae of the fruit fly Drosophila melanogaster.PLoS One. 2011; 6: e25025Crossref PubMed Scopus (122) Google Scholar, MacMillan et al., 2009MacMillan H.A. Guglielmo C.G. Sinclair B.J. Membrane remodeling and glucose in Drosophila melanogaster: a test of rapid cold-hardening and chilling tolerance hypotheses.J. Insect Physiol. 2009; 55: 243-249Crossref PubMed Scopus (45) Google Scholar, Overgaard et al., 2007Overgaard J. Malmendal A. Sørensen J.G. Bundy J.G. Loeschcke V. Nielsen N.C. Holmstrup M. Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster.J. Insect Physiol. 2007; 53: 1218-1232Crossref PubMed Scopus (217) Google Scholar, Overgaard et al., 2005Overgaard J. Sørensen J.G. Petersen S.O. Loeschcke V. Holmstrup M. Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster.J. Insect Physiol. 2005; 51: 1173-1182Crossref PubMed Scopus (202) Google Scholar, Overgaard et al., 2006Overgaard J. Sørensen J.G. Petersen S.O. Loeschcke V. Holmstrup M. Reorganization of membrane lipids during fast and slow cold hardening in Drosophila melanogaster.Physiol. Entomol. 2006; 31: 328-335Crossref Scopus (73) Google Scholar, Qin et al., 2005Qin W. Neal S.J. Robertson R.M. Westwood J.T. Walker V.K. Cold hardening and transcriptional change in Drosophila melanogaster.Insect Mol. Biol. 2005; 14: 607-613Crossref PubMed Scopus (145) Google Scholar, Zhang et al., 2011Zhang J. Marshall K.E. Westwood J.T. Clark M.S. Sinclair B.J. Divergent transcriptomic responses to repeated and single cold exposures in Drosophila melanogaster.J. Exp. Biol. 2011; 214: 4021-4029Crossref PubMed Scopus (86) Google Scholar). Several studies report increases in levels of sugars in response to cold (Colinet et al., 2016Colinet H. Renault D. Javal M. Berková P. Šimek P. Koštál V. Uncovering the benefits of fluctuating thermal regimes on cold tolerance of drosophila flies by combined metabolomic and lipidomic approach.Biochim. Biophys. Acta. 2016; 1861: 1736-1745Crossref PubMed Scopus (38) Google Scholar, Koštál et al., 2011Koštál V. Korbelová J. Rozsypal J. Zahradníčková H. Cimlová J. Tomčala A. Šimek P. Long-term cold acclimation extends survival time at 0 degrees C and modifies the metabolomic profiles of the larvae of the fruit fly Drosophila melanogaster.PLoS One. 2011; 6: e25025Crossref PubMed Scopus (122) Google Scholar, Overgaard et al., 2007Overgaard J. Malmendal A. Sørensen J.G. Bundy J.G. Loeschcke V. Nielsen N.C. Holmstrup M. Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster.J. Insect Physiol. 2007; 53: 1218-1232Crossref PubMed Scopus (217) Google Scholar), although this is not always seen (Kelty and Lee, 2001Kelty J.D. Lee R.E. Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophiladae) during ecologically based thermoperiodic cycles.J. Exp. Biol. 2001; 204: 1659-1666PubMed Google Scholar, MacMillan et al., 2009MacMillan H.A. Guglielmo C.G. Sinclair B.J. Membrane remodeling and glucose in Drosophila melanogaster: a test of rapid cold-hardening and chilling tolerance hypotheses.J. Insect Physiol. 2009; 55: 243-249Crossref PubMed Scopus (45) Google Scholar). Proline accumulates in the cold and has been suggested to act as a cryoprotectant (Koštál et al., 2011Koštál V. Korbelová J. Rozsypal J. Zahradníčková H. Cimlová J. Tomčala A. Šimek P. Long-term cold acclimation extends survival time at 0 degrees C and modifies the metabolomic profiles of the larvae of the fruit fly Drosophila melanogaster.PLoS One. 2011; 6: e25025Crossref PubMed Scopus (122) Google Scholar). However, the fluidity of Drosophila membranes from animals acclimated to different temperatures has never been measured, and the extent to which homeoviscous adaption occurs is unclear. Other cold-blooded animals such as fish increase average fatty acid unsaturation by about 20% upon cold acclimation (Hazel, 1984Hazel J.R. Effects of temperature on the structure and metabolism of cell membranes in fish.Am. J. Physiol. 1984; 246: R460-R470PubMed Google Scholar). However, the evidence for this in Drosophila is equivocal. Many studies report no significant changes in average fatty acid unsaturation in the cold (Colinet et al., 2016Colinet H. Renault D. Javal M. Berková P. Šimek P. Koštál V. Uncovering the benefits of fluctuating thermal regimes on cold tolerance of drosophila flies by combined metabolomic and lipidomic approach.Biochim. Biophys. Acta. 2016; 1861: 1736-1745Crossref PubMed Scopus (38) Google Scholar, Koštál et al., 2011Koštál V. Korbelová J. Rozsypal J. Zahradníčková H. Cimlová J. Tomčala A. Šimek P. Long-term cold acclimation extends survival time at 0 degrees C and modifies the metabolomic profiles of the larvae of the fruit fly Drosophila melanogaster.PLoS One. 2011; 6: e25025Crossref PubMed Scopus (122) Google Scholar, MacMillan et al., 2009MacMillan H.A. Guglielmo C.G. Sinclair B.J. Membrane remodeling and glucose in Drosophila melanogaster: a test of rapid cold-hardening and chilling tolerance hypotheses.J. Insect Physiol. 2009; 55: 243-249Crossref PubMed Scopus (45) Google Scholar, Ohtsu et al., 1998Ohtsu T. Kimura M.T. Katagiri C. How Drosophila species acquire cold tolerance–qualitative changes of phospholipids.Eur. J. Biochem. 1998; 252: 608-611Crossref PubMed Scopus (98) Google Scholar, Overgaard et al., 2008Overgaard J. Tomcala A. Sørensen J.G. Holmstrup M. Krogh P.H. Simek P. Kostál V. Effects of acclimation temperature on thermal tolerance and membrane phospholipid composition in the fruit fly Drosophila melanogaster.J. Insect Physiol. 2008; 54: 619-629Crossref PubMed Scopus (114) Google Scholar). Others observe increases in average unsaturation on the order of 1% (Overgaard et al., 2005Overgaard J. Sørensen J.G. Petersen S.O. Loeschcke V. Holmstrup M. Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster.J. Insect Physiol. 2005; 51: 1173-1182Crossref PubMed Scopus (202) Google Scholar, Overgaard et al., 2006Overgaard J. Sørensen J.G. Petersen S.O. Loeschcke V. Holmstrup M. Reorganization of membrane lipids during fast and slow cold hardening in Drosophila melanogaster.Physiol. Entomol. 2006; 31: 328-335Crossref Scopus (73) Google Scholar). Only one study of Drosophila cold acclimation reports larger changes in unsaturation (Cooper et al., 2012Cooper B.S. Hammad L.A. Fisher N.P. Karty J.A. Montooth K.L. In a variable thermal environment selection favors greater plasticity of cell membranes in Drosophila melanogaster.Evolution. 2012; 66: 1976-1984Crossref PubMed Scopus (39) Google Scholar). The sources of this variability are not understood. One key feature that varies in these studies is diet, which strongly influences the degree of fatty acid unsaturation in membrane phospholipids in Drosophila (Carvalho et al., 2012Carvalho M. Sampaio J.L. Palm W. Brankatschk M. Eaton S. Shevchenko A. Effects of diet and development on the Drosophila lipidome.Mol. Syst. Biol. 2012; 8: 600Crossref PubMed Scopus (182) Google Scholar). Like that of yeast, their key food source, the Drosophila genome encodes only a single Δ9 desaturase, suggesting they cannot introduce double bonds into fatty acids beyond the Δ9 position. Plants can desaturate fatty acids not only at Δ9 but also the Δ12 and Δ15 positions. Flies, like humans, must obtain these fatty acids from the diet in order to produce lipids with poly-unsaturated fatty acids (PUFA) (Carvalho et al., 2012Carvalho M. Sampaio J.L. Palm W. Brankatschk M. Eaton S. Shevchenko A. Effects of diet and development on the Drosophila lipidome.Mol. Syst. Biol. 2012; 8: 600Crossref PubMed Scopus (182) Google Scholar, Randall et al., 2015Randall A.S. Liu C.H. Chu B. Zhang Q. Dongre S.A. Juusola M. Franze K. Wakelam M.J. Hardie R.C. Speed and sensitivity of phototransduction in Drosophila depend on degree of saturation of membrane phospholipids.J. Neurosci. 2015; 35: 2731-2746Crossref PubMed Scopus (39) Google Scholar). Wild Drosophila melanogaster are thought to feed primarily on the yeasts present on decomposing fruit. Olfactory and gustatory cues attract them to yeasts, both as a food source and as a substrate for egg laying. Although they can detect plant compounds derived from leaves or unripe fruit, these are less attractive than yeast or are even aversive (Becher et al., 2012Becher P.G. Flick G. Rozpędowska E. Schmidt A. Hagman A. Lebreton S. Larsson M.C. Hansson B.S. Piškur J. Witzgall P. et al.Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development.Funct. Ecol. 2012; 26: 822-828Crossref Scopus (262) Google Scholar, Hoang et al., 2015Hoang D. Kopp A. Chandler J.A. Interactions between Drosophila and its natural yeast symbionts-Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship?.PeerJ. 2015; 3: e1116Crossref PubMed Scopus (43) Google Scholar, Koštál et al., 2012Koštál V. Šimek P. Zahradníčková H. Cimlová J. Štětina T. Conversion of the chill susceptible fruit fly larva (Drosophila melanogaster) to a freeze tolerant organism.Proc. Natl. Acad. Sci. USA. 2012; 109: 3270-3274Crossref PubMed Scopus (108) Google Scholar, Stensmyr et al., 2003Stensmyr M.C. Giordano E. Balloi A. Angioy A.M. Hansson B.S. Novel natural ligands for Drosophila olfactory receptor neurones.J. Exp. Biol. 2003; 206: 715-724Crossref PubMed Scopus (138) Google Scholar, Versace et al., 2016Versace E. Eriksson A. Rocchi F. Castellan I. Sgadò P. Haase A. Physiological and behavioral responses in Drosophila melanogaster to odorants present at different plant maturation stages.Physiol. Behav. 2016; 163: 322-331Crossref PubMed Scopus (8) Google Scholar). It is unclear to what extent they consume plants and, if so, whether it is important. We recently developed two different food recipes containing exclusively yeast or plant material. These foods contain similar proportions of calories derived from protein, lipid, and carbohydrate but differ in their lipid composition (Brankatschk et al., 2014Brankatschk M. Dunst S. Nemetschke L. Eaton S. Delivery of circulating lipoproteins to specific neurons in the Drosophila brain regulates systemic insulin signaling.Elife. 2014; 3https://doi.org/10.7554/eLife.02862Crossref PubMed Scopus (53) Google Scholar, Carvalho et al., 2012Carvalho M. Sampaio J.L. Palm W. Brankatschk M. Eaton S. Shevchenko A. Effects of diet and development on the Drosophila lipidome.Mol. Syst. Biol. 2012; 8: 600Crossref PubMed Scopus (182) Google Scholar). Yeast glycerolipids contain saturated or mono-unsaturated fatty acids (MUFAs) with 14–18 carbon units, while plant lipids also contain longer and PUFAs. Plant food contains phytosterols, while yeast food contains fungal sterols (Buttke et al., 1980Buttke T.M. Jones S.D. Bloch K. Effect of sterol side chains on growth and membrane fatty acid composition of Saccharomyces cerevisiae.J. Bacteriol. 1980; 144: 124-130PubMed Google Scholar, Carvalho et al., 2012Carvalho M. Sampaio J.L. Palm W. Brankatschk M. Eaton S. Shevchenko A. Effects of diet and development on the Drosophila lipidome.Mol. Syst. Biol. 2012; 8: 600Crossref PubMed Scopus (182) Google Scholar). Larvae fed with these two different diets have different lipidomes, and only plant-fed larvae accumulate significant amounts of phospholipids containing PUFAs (Carvalho et al., 2012Carvalho M. Sampaio J.L. Palm W. Brankatschk M. Eaton S. Shevchenko A. Effects of diet and development on the Drosophila lipidome.Mol. Syst. Biol. 2012; 8: 600Crossref PubMed Scopus (182) Google Scholar). The different lipids present in plant and yeast food influence not only membrane lipid composition but also developmental rate, fertility, and lifespan (Brankatschk et al., 2014Brankatschk M. Dunst S. Nemetschke L. Eaton S. Delivery of circulating lipoproteins to specific neurons in the Drosophila brain regulates systemic insulin signaling.Elife. 2014; 3https://doi.org/10.7554/eLife.02862Crossref PubMed Scopus (53) Google Scholar, Carvalho et al., 2012Carvalho M. Sampaio J.L. Palm W. Brankatschk M. Eaton S. Shevchenko A. Effects of diet and development on the Drosophila lipidome.Mol. Syst. Biol. 2012; 8: 600Crossref PubMed Scopus (182) Google Scholar). Plant-fed animals develop more slowly than yeast-fed animals, and adults live longer on a plant diet. These differences in developmental rate and lifespan are due to changes in systemic insulin/IGF (insulin-like growth factor)-like signaling (IIS). Yeast lipids, but not plant lipids, cause lipoproteins to accumulate on specific CNS neurons that connect to insulin producing cells (IPCs) (Brankatschk et al., 2014Brankatschk M. Dunst S. Nemetschke L. Eaton S. Delivery of circulating lipoproteins to specific neurons in the Drosophila brain regulates systemic insulin signaling.Elife. 2014; 3https://doi.org/10.7554/eLife.02862Crossref PubMed Scopus (53) Google Scholar). When this happens, these neurons activate IPCs, causing them to release Drosophila insulin-like peptides (Dilps). Dilps elevate systemic IIS, speed development, increase fertility, and shorten lifespan (Brankatschk et al., 2014Brankatschk M. Dunst S. Nemetschke L. Eaton S. Delivery of circulating lipoproteins to specific neurons in the Drosophila brain regulates systemic insulin signaling.Elife. 2014; 3https://doi.org/10.7554/eLife.02862Crossref PubMed Scopus (53) Google Scholar, Garofalo, 2002Garofalo R.S. Genetic analysis of insulin signaling in Drosophila.Trends Endocrinol. Metab. 2002; 13: 156-162Abstract Full Text Full Text PDF PubMed Scopus (275) Google Scholar, Giannakou and Partridge, 2007Giannakou M.E. Partridge L. Role of insulin-like signalling in Drosophila lifespan.Trends Biochem. Sci. 2007; 32: 180-188Abstract Full Text Full Text PDF PubMed Scopus (209) Google Scholar). Why should yeast-derived lipids elevate IIS independent of the caloric content of the diet? We speculated that such a mechanism might have evolved to allow Drosophila to maximally exploit summer blooms of yeasts in the wild. Interestingly, distinct alleles of the Drosophila insulin receptor and other components of the insulin signaling pathway have been shown to vary in frequency according to latitude and even according to season (Fabian et al., 2012Fabian D.K. Kapun M. Nolte V. Kofler R. Schmidt P.S. Schlötterer C. Flatt T. Genome-wide patterns of latitudinal differentiation among populations of Drosophila melanogaster from North America.Mol. Ecol. 2012; 21: 4748-4769Crossref PubMed Scopus (172) Google Scholar, Paaby et al., 2014Paaby A.B. Bergland A.O. Behrman E.L. Schmidt P.S. A highly pleiotropic amino acid polymorphism in the Drosophila insulin receptor contributes to life-history adaptation.Evolution. 2014; 68: 3395-3409Crossref PubMed Scopus (65) Google Scholar). We wondered whether plant-derived food components might have important functions under different conditions. For example, since Drosophila melanogaster cannot produce lipids with PUFAs unless they consume plants, we wondered whether plant food might help flies adjust their membrane biophysical properties to survive low temperatures in the winter. Yeast-derived olfactory cues attract Drosophila and stimulate feeding and egg laying (Becher et al., 2012Becher P.G. Flick G. Rozpędowska E. Schmidt A. Hagman A. Lebreton S. Larsson M.C. Hansson B.S. Piškur J. Witzgall P. et al.Yeast, not fruit volatiles mediate Drosophila melanogaster attraction, oviposition and development.Funct. Ecol. 2012; 26: 822-828Crossref Scopus (262) Google Scholar, Hoang et al., 2015Hoang D. Kopp A. Chandler J.A. Interactions between Drosophila and its natural yeast symbionts-Is Saccharomyces cerevisiae a good model for studying the fly-yeast relationship?.PeerJ. 2015; 3: e1116Crossref PubMed Scopus (43) Google Scholar, Koštál et al., 2012Koštál V. Šimek P. Zahradníčková H. Cimlová J. Štětina T. Conversion of the chill susceptible fruit fly larva (Drosophila melanogaster) to a freeze tolerant organism.Proc. Natl. Acad. Sci. USA. 2012; 109: 3270-3274Crossref PubMed Scopus (108) Google Scholar, Stensmyr et al., 2003Stensmyr M.C. Giordano E. Balloi A. Angioy A.M. Hansson B.S. Novel natural ligands for Drosophila olfactory receptor neurones.J. Exp. Biol. 2003; 206: 715-724Crossref PubMed Scopus (138) Google Scholar, Versace et al., 2016Versace E. Eriksson A. Rocchi F. Castellan I. Sgadò P. Haase A. Physiological and behavioral responses in Drosophila melanogaster to odorants present at different plant maturation stages.Physiol. Behav. 2016; 163: 322-331Crossref PubMed Scopus (8) Google Scholar). Although Drosophila clearly prefer yeast to plant-derived compounds at moderate temperatures, we wondered whether this preference might be temperature dependent. Indeed, when females of the wild-type strain OregonR are shifted to 15°C, they begin to lay eggs near plant food rather than yeast food (Figures 1A, 1B, S1A, and S1B), although they still feed on yeast (Figures 1C and S1C–S1E). At 12°C, they shift their feeding preference to plant food after a short feeding hiatus (Figures 1C and S1C–S1E). The feeding and egg laying assays require several days to perform. To investigate how rapidly temperature influences attraction to different foods, we presented flies with a choice of plant or yeast food and filmed them as the temperature decreased from 21°C to 11°C over the course of 3 hr (Figures 1D–1D″; Video S1). As expected, flies spent more time near yeast food at 21°C. As the temperature reached 16°C (after about 40 min), flies tended to occupy regions in the middle of the plate—away from both the plant and yeast food. By the time the temperature reached 11°C, flies tended to cluster near plant food. Thus, the relative attractiveness of yeast and plant food changes rapidly as temperature drops. eyJraWQiOiI4ZjUxYWNhY2IzYjhiNjNlNzFlYmIzYWFmYTU5NmZmYyIsImFsZyI6IlJTMjU2In0.eyJzdWIiOiI4YjM1ODVmNjA2NDQxNTk1NTJmMmM1NjgyMThiOTJmMCIsImtpZCI6IjhmNTFhY2FjYjNiOGI2M2U3MWViYjNhYWZhNTk2ZmZjIiwiZXhwIjoxNjc5Mjc1NjQ0fQ.J-SlCXfx65n66Q-QclmPy3_A52dmZpugbvzHaq-eB9Tvqa8wliYhpx602JA8VXZnmYSvQevdYRDb9t6PsMbLTOUa6ugqD2W_5gj3RhSaY7fCLlWeXfHDbiqE6oUCq_BiZz10IUtbizMeEmmzDqfrAzye38weIPe7IcIvuFAgzkpXePlAgDo6JO6p4QMJCUozwYm0GgkWivb5XoWOlge8uTh-RKQJKVN2bi3Pte5u-EeOvybL0gC-7YkrhPnBR0K-qoyH2G_IGfc7iw4bTenlwbpaHN1OWVlOxsDaoIjiCdjnJet8NnAzhdJGkLD5_cgPBZpn0-n7lSlPKXlPCfX0pw Download .mp4 (5.72 MB) Help with .mp4 files Video S1. Wild-Type Flies in Food Choice Assays at Changing Temperatures, Related to Figure 1Plant food is yellow and yeast food appears brown We wondered whether olfactory cues were important for low temperature food choice. To address this, we performed the same experiment using orb83 mutant flies. Orb83 is needed for dendritic localization of odorant receptors and its loss disrupts many odorant responses (Larsson et al., 2004Larsson M.C. Domingos A.I. Jones W.D. Chiappe M.E. Amrein H. Vosshall L.B. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction.Neuron. 2004; 43: 703-714Abstract Full Text Full Text PDF PubMed Scopus (934) Google Scholar). Flies mutant for orb83 spend more time near the rim of the plates and do not congregate around either plant or yeast food at any temperature (Figures 1E–1E″; Video S2). This suggests that the preference for plant food depends either on plant-specific odorants that become attractive at low temperature or on a changed and aversive response to compounds derived from yeast. eyJraWQiOiI4ZjUxYWNhY2IzYjhiNjNlNzFlYmIzYWFmYTU5NmZmYyIsImFsZyI6IlJTMjU2In0.eyJzdWIiOiI2NzkyYTVjYTVkZjI0N2QwNDAyZGZlYzAxMDI1YmFkOSIsImtpZCI6IjhmNTFhY2FjYjNiOGI2M2U3MWViYjNhYWZhNTk2ZmZjIiwiZXhwIjoxNjc5Mjc1NjQ0fQ.JyLDgx-4eCba4ZrAKZwNWpY6qoIxwTcCPfwxf1mKx-gqpONKX16nZWu7NCxGaSdchHsldoHHKEDcTtvaeU1Cd27aousqHCFr1RPA2AHGHHziEeFbE1H-1-yw9mq7Dav8WBOMix8HxPCq0_JkQO7PuX5CqMjUxQU6UhAtvS68HamobtQOXgyhcN5ZvLIkDySgLVKdbzf3dleEtF5erF7qhmibKhz-CUDNEbuNTzmYBc5gziR5s-TJi-VNuy7qN-8Mc1PDfZEJzy6AuwPmD83xDXDEZvsIhNYwEJkl1J9r8VVIg615s8FWM24IrtaFxG4ToU78waG0GbqTCJ7P9mJBbA Download .mp4 (4.89 MB) Help with .mp4 files Video S2. or83b Mutant Flies in Food Choice Assays at Changing Temperatures, Related to Figure 1Plant food is yellow and yeast food appears brown To inv" @default.
• W2893389670 created "2018-10-05" @default.
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• W2893389670 date "2018-09-01" @default.
• W2893389670 modified "2023-10-14" @default.
• W2893389670 title "A Temperature-Dependent Switch in Feeding Preference Improves Drosophila Development and Survival in the Cold" @default.
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• W2893389670 doi "https://doi.org/10.1016/j.devcel.2018.05.028" @default.
• W2893389670 hasPubMedId "https://pubmed.ncbi.nlm.nih.gov/30352177" @default.
• W2893389670 hasPublicationYear "2018" @default.
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