Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster

Functional Ecology

Volumn 26, Issue 1, 2012, Pages 84-93

  Colinet, Hervé ^a,b,c   Hoffmann, Ary A ^b  

^a EARTH AND LIFE INSTITUTE   (Belgium)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Acclimation; Chilling injuries; Cold stress; Drosophila melanogaster; Frost; Hsp; Phenotypic plasticity; Starvin

Indexed keywords

ACCLIMATION; ADAPTATION; COLD AIR; COMPARATIVE STUDY; DEVELOPMENTAL BIOLOGY; ENVIRONMENTAL STRESS; FLY; INJURY; MOLECULAR ANALYSIS; NUMERICAL MODEL; PHENOTYPIC PLASTICITY; TEMPERATURE EFFECT; TEMPORAL VARIATION; TOLERANCE;

DROSOPHILA MELANOGASTER;

EID: 84856018412     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2011.01898.x     Document Type: Article

References (53)

1. Angilletta, M.J. Jr (2009) Thermal Adaptation. A Theoretical and Empirical Synthesis. Oxford University Press, Oxford.
2. Ayrinhac, A., Debat, V., Gibert, P., Kister, A.G., Legout, H., Moreteau, B., Vergilino, R. & David, J.R. (2004) Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Functional Ecology, 18, 700-706.
3. Bahrndorff, S., Mariën, J., Loeschcke, V. & Ellers, J. (2009) Dynamics of heat-induced thermal stress resistance and Hsp70 expression in the springtail, Orchesella cincta. Functional Ecology, 23, 233-239.
4. Chen, C.P. & Walker, V.K. (1994) Cold-shock and chilling tolerance in Drosophila. Journal of Insect Physiology, 40, 661-669.
5. Chown, S.L. & Nicolson, S.W. (2004) Insect Physiological Ecology: Mechanisms and Patterns. Oxford University Press, Oxford.
6. Chown, S.L. & Terblanche, J.S. (2006) Physiological diversity in insects: ecological and evolutionary contexts. Advances in Insect Physiology, 33, 50-152.
7. Cobreros, L., Fernández-Miñán, A., Luque, C.M., González-Reyes, A. & Martín-Bermudo, M.D. (2008) A role for the chaperone Hsp70 in the regulation of border cell migration in the Drosophila ovary. Mechanisms of Development, 125, 1048-1058.
8. Colinet, H. & Hoffmann, A.A. (2010) Gene and protein expression of Drosophila Starvin during cold stress and recovery from chill coma. Insect Biochemistry & Molecular Biology, 40, 425-428.
9. Colinet, H., Lee, S.F. & Hoffmann, A.A. (2010a) Temporal expression of heat shock genes during cold stress and recovery from chill coma in adult Drosophila melanogaster. FEBS Journal, 277, 174-185.
10. Colinet, H., Lee, S.F. & Hoffmann, A.A. (2010b) Knocking down expression of Hsp22 and Hsp23 by RNA interference affects recovery from chill coma in Drosophila melanogaster. Journal of Experimental Biology, 213, 4146-4150.
11. Colinet, H., Lee, S.F. & Hoffmann, A.A. (2010c) Functional characterization of the Frost gene in Drosophila melanogaster: importance for recovery from chill coma. PLoS ONE, 5, e10925.
12. Fischer, K. & Karl, I. (2010) Exploring plastic and genetic responses to temperature variation using copper butterflies. Climate Research, 43, 17-30.
13. Fischer, K., Dierks, A., Franke, K., Geister, T.L., Liszka, M., Winter, S. & Pflicke, C. (2010) Environmental effects on temperature stress resistance in the tropical butterfly Bicyclus Anynana. PLoS ONE, 5, e15284.
14. Hoffmann, A.A., Anderson, A. & Hallas, R. (2002) Opposing clines for high and low temperature resistance in Drosophila melanogaste. Ecology Letters, 5, 614-618.
15. Hoffmann, A.A., Shirriffs, J. & Scott, M. (2005) Relative importance of plastic vs genetic factors in adaptive differentiation: geographical variation for stress resistance in Drosophila melanogaster from eastern Australia. Functional Ecology, 19, 222-227.
16. 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.
17. Jensen, D., Overgaard, J. & Sørensen, J.G. (2007) The influence of developmental stage on cold shock resistance and ability to cold-harden in Drosophila melanogaster. Journal of Insect Physiology, 53, 179-186.
18. Kelty, J. (2007) Rapid cold-hardening of Drosophila melanogaster in a field setting. Physiological Entomology, 32, 343-350.
19. Kelty, J.D. & Lee, R.E. Jr (2001) Rapid cold-hardening of Drosophila melanogaster (Diptera: Drosophilidae) during ecologically based thermoperiodic cycles. Journal of Experimental Biology, 204, 1659-1666.
20. Kostál, V. & Tollarová-Borovanská, M. (2009) The 70kDa heat shock protein assists during the repair of chilling injury in the insect, Pyrrhocoris apterus. PLoS ONE, 4, e4546.
21. Kristensen, T.N., Hoffmann, A.A., Overgaard, J., Sørensen, J.G., Hallas, R. & Loeschcke, V. (2008) Costs and benefits of cold acclimation in field-released Drosophila. Proceedings of the National Academy of Sciences USA, 105, 216-221.
22. Larsen, K.J. & Lee, R.E. (1994) Cold tolerance including rapid cold-hardening and inoculative freezing of fall migrant monarch butterflies in Ohio. Journal of Insect Physiology, 40, 859-864.
23. Lee, R.E. Jr & Denlinger, D.L. (2010) Rapid cold hardening: ecological significance and underpinning mechanisms. Low Temperature Biology of Insects (eds D.L. Denlinger & R.E. Lee Jr), pp. 35-58, Cambridge University Press, Cambridge.
24. Lee, M.T., Kuo, F.C., Whitmore, G.A. & Sklar, J. (2000) Importance of replication in microarray gene expression studies: statistical methods and evidence from repetitive cDNA hybridizations. Proceedings of the National Academy of Sciences USA, 97, 9834-9839.
25. Li, Y., Gong, H. & Park, H.Y. (1999) Characterization of rapid cold-hardening response in the overwintering mature larvae of pine needle gall midge, Thecopidiplosis japonensis. Cryo Letters, 20, 383-392.
26. Loeschcke, V. & Sørensen, J.G. (2005) Acclimation, heat shock and hardening-a response from evolutionary biology. Journal of Thermal Biology, 30, 255-257.
27. Macmillan, H.A. & Sinclair, B.J. (2011) Mechanisms underlying insect chill-coma. Journal of Insect Physiology, 57, 12-20.
28. Marais, E. & Chown, S.L. (2008) Beneficial acclimation and the Bogert effect. Ecology Letters, 11, 1027-1036.
29. McDonald, J.R., Bale, J.S. & Walters, K.F.A. (1997) Rapid cold hardening in the western flower thrips Frankliniella occidentalis. Journal of Insect Physiology, 43, 759-766.
30. Michaud, M.R. & Denlinger, D.L. (2010) Genomics, proteomics and metabolomics: finding the other players in insect cold-tolerance. Low Temperature Biology of Insects (eds D.L. Denlinger & R.E. Lee Jr), pp. 91-116, University Press Cambridge, Cambridge.
31. Nielsen, M.M., Overgaard, J., Sørensen, J.G., Holmstrup, M., Justesen, J. & Loeschcke, V. (2005) Role of HSF activation for resistance to heat, cold and high-temperature knock-down. Journal of Insect Physiology, 51, 1320-1329.
32. Overgaard, J., Sørensen, 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., Malmendal, A., Sørensen, J.G., Bundy, J.G., Loeschcke, V., Nielsen, N.C. & Holmstrup, M. (2007) Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. Journal of Insect Physiology, 53, 1218-1232.
34. Overgaard, J., Tomcala, A., Sørensen, J.G., Holmstrup, M., Krogh, P.H., Simek, P. & Kostal, V. (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. Petavy, G., David, J.R., Gibert, P. & Moreteau, B. (2001) Viability and rate of development at different temperatures in Drosophila: a comparison of constant and alternating thermal regimes. Journal of Thermal Biology, 26, 29-39.
36. Piersma, T. & Drent, J. (2003) Phenotypic flexibility and the evolution of organismal design. Trends in Ecology and Evolution, 18, 228-233.
37. Powell, S.J. & Bale, J.S. (2005) Low temperature acclimated populations of the grain aphid Sitobion avenae retain ability to rapidly cold harden with enhanced fitness. Journal of Experimental Biology, 208, 2615-2620.
38. Powell, S.J. & Bale, J.S. (2006) Effect of long-term and rapid cold hardening on the cold torpor temperature of an aphid. Physiological Entomology, 31, 348-352.
39. Promislow, D.E.L., Tatar, M., Khazaeli, A.A. & Curtsinger, J.W. (1996) Age-specific patterns of genetic variance in Drosophila melanogaster. I. Mortality. Genetics, 143, 839-848.
40. Qin, W., Neal, S., Robertson, R., Westwood, J. & Walker, V. (2005) Cold hardening and transcriptional change in Drosophila melanogaster. Insect Molecular Biology, 14, 607-613.
41. Rajamohan, A. & Sinclair, B.J. (2009) Hardening trumps acclimation in improving cold tolerance of Drosophila melanogaster larvae. Physiological Entomology, 34, 217-223.
42. Rako, L. & Hoffmann, A.A. (2006) Complexity of the cold acclimation response in Drosophila melanogaster. Journal of Insect Physiology, 52, 94-104.
43. Rinehart, J.P., Li, A., Yocum, G.D., Robich, R.M., Hayward, S.A. & Denlinger, D.L. (2007) Up-regulation of heat shock proteins is essential for cold survival during insect diapause. Proceedings of the National Academy of Sciences USA, 104, 11130-11137.
44. Shintani, Y. & Ishikawa, Y. (2007) Relationship between rapid cold-hardening and cold acclimation in the eggs of the yellow-spotted longicorn beetle, Psacothea hilaris. Journal of Insect Physiology, 53, 1055-062.
45. Sinclair, B.J. & Roberts, S.P. (2005) Acclimation, shock and hardening in the cold. Journal of Thermal Biology, 30, 557-562.
46. Sørensen, J.G., Kristensen, T.N. & Loeschcke, V. (2003) The evolutionary and ecological role of heat shock proteins. Ecology Letters, 6, 1025-1037.
47. Sørensen, J.G., Michalak, P., Justesen, J. & Loeschcke, V. (1999) Expression of the heat-shock protein HSP70 in Drosophila buzzatii lines selected for thermal resistance. Hereditas, 131, 155-164.
48. Taylor, F. (1981) Ecology and evolution of physiological time in insects. The American Naturalist, 117, 1-23.
49. Terblanche, J.S. & Chown, S.L. (2006) The relative contributions of developmental plasticity and adult acclimation to physiological variation in the tsetse fly, Glossina pallidipes (Diptera, Glossinidae). Journal of Experimental Biology, 209, 1064-1073.
50. Terblanche, J.S., Marais, E. & Chown, S.L. (2007) Stage-related variation in rapid cold hardening as a test of the environmental predictability hypothesis. Journal of Insect Physiology, 53, 455-462.
51. Wang, H., Zhongren, L., Xue, L. & Oetting, R.D. (2011) Rapid cold hardening and expression of heat shock protein genes in the b-biotype Bemisia tabaci. Environmental Entomology, 40, 132-139.
52. Watson, M.J.O. & Hoffmann, A.A. (1996) Acclimation, cross-generation effects, and the response to selection for increased cold resistance in Drosophila. Evolution, 50, 1182-1192.
53. Wilson, R.S. & Franklin, C.E. (2002) Testing the beneficial acclimation hypothesis. Trends in Ecology and Evolution, 17, 66-70.