Thermal adaptation of cellular membranes in natural populations of Drosophila melanogaster

Functional Ecology

Volumn 28, Issue 4, 2014, Pages 886-894

  Cooper, Brandon S ^a   Hammad, Loubna A ^a   Montooth, Kristi L ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Acclimation; Cellular membranes; Drosophila melanogaster; Homeoviscous adaptation; Phenotypic plasticity; Thermal adaptation

Indexed keywords

ACCLIMATION; ADAPTATION; ALLELE; CELL ORGANELLE; DATA SET; FLY; MEMBRANE; NUMERICAL MODEL; ORGANIC COMPOUND; PHYSIOLOGICAL RESPONSE; POPULATION STRUCTURE; TEMPERATURE EFFECT;

UNITED STATES;

DROSOPHILA MELANOGASTER;

EID: 84904363045     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/1365-2435.12264     Document Type: Article

References (47)

1. Agrawal, A.F. & Stinchcombe, J.R. (2009) How much do genetic covariances alter the rate of adaptation? Proceedings of the Royal Society B-Biological Sciences, 276, 1183-1191.
2. Angilletta, M.J., Bennett, A.F., Guderley, H., Navas, C.A., Seebacher, F. & Wilson, R.S. (2006) Coadaptation: a unifying principle in evolutionary thermal biology. Physiological and Biochemical Zoology, 79, 282-294.
3. Condon, C.H., Cooper, B.S., Yeaman, S. & Angilletta, M.J. (2014) Temporal variation favors the evolution of generalists in experimental populations of Drosophila melanogaster. Evolution, 68, 720-728.
4. Cooper, B.S., Czarnoleski, M. & Angilletta, M.J. (2010) Acclimation of thermal physiology in natural populations of Drosophila melanogaster: a test of an optimality model. Journal of Evolutionary Biology, 23, 2346-2355.
5. Cooper, B.S., Hammad, L.A., Fisher, N.P., Karty, J.A. & Montooth, K.L. (2012) In a variable thermal environment selection favors greater plasticity of cell membranes in Drosophila melanogaster. Evolution, 66, 1976-1984.
6. David, J.R. & Capy, P. (1988) Genetic variation of Drosophila melanogaster natural populations. Trends in Genetics, 4, 106-111.
7. Dillon, M.E., Wang, G., Garrity, P.A. & Huey, R.B. (2009) Thermal preference in Drosophila. Journal of Thermal Biology, 34, 109-119.
8. Dobrosotskaya, I.Y., Seegmiller, A.C., Brown, M.S., Goldstein, J.L. & Rawson, R.B. (2002) Regulation of SREBP processing and membrane lipid production by phospholipids in Drosophila. Science, 296, 879-883.
9. Feder, M.E., Blair, N. & Figueras, H. (1997) Natural thermal stress and heat-shock protein expression in Drosophila larvae and pupae. Functional Ecology, 11, 90-100.
10. Folch, J., Lees, M. & Stanley, G.H.S. (1957) A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226, 497-509.
11. Gabriel, W. & Lynch, M. (1992) The selective advantage of reaction norms for environmental tolerance. Journal of Evolutionary Biology, 5, 41-59.
12. Gabriel, W., Luttbeg, B., Sih, A. & Tollrian, R. (2005) Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. American Naturalist, 166, 339-353.
13. Gilchrist, G.W. (1995) Specialists and generalists in changing environments. I. Fitness landscapes of thermal sensitivity. American Naturalist, 146, 252-270.
14. Gomulkiewicz, R. & Kirkpatrick, M. (1992) Quantitative genetics and the evolution of reaction norms. Evolution, 46, 390-411.
15. Hammad, L.A., Cooper, B.S., Fisher, N.P., Montooth, K.L. & Karty, J.A. (2011) Profiling and quantification of Drosophila melanogaster lipids using liquid chromatography/mass spectrometry. Rapid Communications in Mass Spectrometry, 25, 2959-2968.
16. Hazel, J.R. (1995) Thermal adaptation in biological membranes: is homeoviscous adaptation the explanation? Annual Review of Physiology, 57, 19-42.
17. Hochochka, P.W. & Somero, G.N. (2002) Biochemical Adaptation. Oxford University Press, Oxford.
18. Hoffmann, A.A., Sørensen, J.G. & Loeschcke, V. (2003) Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. Journal of Thermal Biology, 28, 175-216.
19. Huey, R.B., Hertz, P.E. & Sinervo, B. (2003) Behavioral drive versus behavioral inertia in evolution: a null model approach. American Naturalist, 161, 357-366.
20. Jones, H.E., Harwood, J.L., Bowen, I.D. & Griffiths, G. (1992) Lipid composition of subcellular membranes from larvae and prepupae of Drosophila melanogaster. Lipids, 27, 984-987.
21. Kassen, R. (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology, 15, 173-190.
22. Kawecki, T.J. (1994) Accumulation of deleterious mutations and the evolutionary cost of being a generalist. The American Naturalist, 144, 833-838.
23. Kostal, V. & Simek, P. (1998) Changes in fatty acid composition of phospholipids and triacylglycerols after cold-acclimation of an aestivating insect prepupa. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 168, 453-460.
24. Levins, R. (1968) Evolution in Changing Environments: Some Theoretical Explorations. Princeton University Press, Princeton.
25. Lynch, M.J. & Gabriel, W. (1987) Environmental tolerance. American Naturalist, 129, 283-303.
26. MacMillan, H.A., Guglielmo, C.G. & Sinclair, B.J. (2009) Membrane remodeling and glucose in Drosophila melanogaster: a test of rapid cold-hardening and chilling tolerance hypotheses. Journal of Insect Physiology, 55, 243-249.
27. Miller, R.R., Yates, J.W. & Geer, B.W. (1993) Dietary ethanol stimulates the activity of phosphatidylcholine specific phospholipase D and the formation of phosphatidylethanol in Drosophila melaongaster larvae. Insect Biochemistry and Molecular Biology, 23, 749-755.
28. Montooth, K.L., Siebenthall, K.T. & Clark, A.G. (2006) Membrane lipid physiology and toxin catabolism underlie ethanol and acetic acid tolerance in Drosophila melanogaster. Journal of Experimental Biology, 209, 3837-3850.
29. Moran, N.A. (1994) Adaptation and constraint in the complex life cycles of animals. Annual Review of Ecology and Systematics, 25, 573-600.
30. Nilsson-Ortman, V., Stoks, R., De Block, M. & Johansson, F. (2012) Generalists and specialists along a latitudinal transect: patterns of thermal adaptation in six species of damselflies. Ecology, 93, 1340-1352.
31. Ohtsu, T., Kimura, M.T. & Katagiri, C. (1998) How Drosophila species acquire cold tolerance: qualitative changes of phospholipids. European Journal of Biochemistry, 252, 608-611.
32. Overgaard, J., Sorensen, J.G., Petersen, S.O., Loeschcke, V. & Holmstrup, M. (2005) Changes in membrane lipid composition following rapid cold hardening in Drosophila melanogaster. Journal of Insect Physiology, 51, 1173-1182.
33. Overgaard, J., Sorensen, J.G., Petersen, S.O., Loeschcke, V. & Holmstrup, M. (2006) Reorganization of membrane lipids during fast and slow cold hardening in Drosophila melanogaster. Physiological Entomology, 31, 328-335.
34. Overgaard, J., Tomcala, A., Sorensen, J.G., Holmstrup, M., Krogh, P.H., Simek, P. et al. (2008) Effects of acclimation temperature on thermal tolerance and membrane phospholipid composition in the fruit fly Drosophila melanogaster. Journal of Insect Physiology, 54, 619-629.
35. R Core Team(2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
36. Rawson, R.B. (2003) The SREBP pathway - insights from insigs and insects. Nature Reviews Molecular Cell Biology, 4, 631-640.
37. Reboud, X. & Bell, G. (1997) Experimental evolution in Chlamydomonas. 3. Evolution of specialist and generalist types in environments that vary in space and time. Heredity, 78, 507-514.
38. Robertson, J.C. & Hazel, J.R. (1995) Cholesterol content of trout plasma-membranes varies with acclimation temperature. American Journal of Physiology-Regulatory Integrative and Comparative Physiology, 38, R1113-R1119.
39. Scheitz, C.J.F., Guo, Y., Early, A.M., Harshman, L.G. & Clark, A.G. (2013) Heritability and inter-populational differences in lipid profiles of Drosophila melanogaster. PLoS ONE, 8, e72726.
40. Shreve, S.M., Yi, S.-X. & Lee, R.E. Jr (2007) Increased dietary cholesterol enhances cold tolerance in Drosophila melanogaster. Cryoletters, 28, 33-37.
41. Sinensky, M. (1974) Homeoviscous adaptation - homeostatic process that regulates viscosity of membrane lipids in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America, 71, 522-525.
42. van Tienderen, P.H. (1991) Evolution of generalists and specialists in spatially heterogeneous environments. Evolution, 45, 1317-1331.
43. Van Dyken, J.D. & Wade, M.J. (2009) The genetic signature of conditional expression. Genetics, 184, 557-570.
44. Via, S. (1993) Adaptive phenotypic plasticity - target of byproduct of selection in a variable environment. American Naturalist, 142, 352-365.
45. Via, S. & Lande, R. (1985) Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution, 39, 505-522.
46. Whitlock, M.C. (1996) The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. The American Naturalist, 148, S65-S77.
47. Zehmer, J.K. & Hazel, J.R. (2003) Plasma membrane rafts of rainbow trout are subject to thermal acclimation. Journal of Experimental Biology, 206, 1657-1667.