Keeping pace with climate change: What is wrong with the evolutionary potential of upper thermal limits?

Ecology and Evolution

Volumn 2, Issue 11, 2012, Pages 2866-2880

  Santos, Mauro ^a   Castañeda, Luis E ^a,b   Rezende, Enrico L ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSIDAD AUSTRAL DE CHILE   (Chile)

Author keywords

Ctmax; Heating rate; Knockdown resistance; Metabolic rate; Selection responses; Thermotolerance

Indexed keywords

EID: 84880137018     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.385     Document Type: Article

References (81)

1. Addo-Bediako, A., S. L. Chown, and K. J. Gaston. 2000 Thermal tolerance, climatic variability and latitude. Proc R. Soc. London B 267:739-745
2. Angilletta, M. J., Jr. 2009. Thermal adaptation. A theoretical and empirical synthesis. Oxford Univ. Press, Oxford
3. Berrigan, D., and L. Partridge. 1997. Influence of temperature and activity on the metabolic rate of adult Drosophila melanogaster. Comp. Bioch. Physiol. 118A:1301-1307
4. Block, W., N. R. Webb, S. Coulson, I. D. Hodkinson, and M. R. Worland. 1994. Thermal adaptation in the Arctic collembolan Onychiurus arcticus (Tullberg). J. Insect Physiol 40:715-722
5. Blows, M. W., and A. A. Hoffmann. 2005. A reassessment of genetic limits to evolutionary change. Ecology 86:1371-1384
6. Bubli, O. A., A. G. Imasheva, and V. Loeschcke. 1998 Selection for knockdown resistance to heat in Drosophila melanogaster at high and low larval densities. Evolution 52:619-625
7. Bulmer, M. G. 1971. The effect of selection on genetic variability. Am. Nat. 105:201-211
8. Bulmer, M. G. 1976. The effect of selection on genetic variability: a simulation study. Genet. Res. 28:101-117
9. Castañeda, L. E., G. Calabria, L. A. Betancourt, E. L. Rezende, and M. Santos. 2012. Measurement error in heat tolerance assays. J. Therm. Biol 37:432-437
10. Cavicchi, S., D. Guerra, V. Latorre, and R. B. Huey. 1995 Chromosomal analysis of heat-shock tolerance in Drosophila melanogaster evolving at different temperatures in the laboratory. Evolution 49:676-684
11. Chevin, L.-M., R. Lande, and G. M. Mace. 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8(4):e1000357
12. Chidawanyika, F., and J. S. Terblanche. 2011. Rapid thermal responses and thermal tolerance in adult codling moth Cydia pomonella (Lepidoptera: Tortricidae). J. Insect Physiol. 57:108-117
13. Chown, S. L., K. R. Jumbam, J. G. Sørensen, and J. S Terblanche. 2009. Phenotypic variance, plasticity and heritability estimates of critical thermal limits depend on methodological context. Funct. Ecol. 23: 133-140
14. Chown, S. L., A. A. Hoffmann, T. N. Kristensen, M. J Angilletta, N. C. Stenseth, and C. Pertoldi. 2010. Adapting to climate change: a perspective from evolutionary physiology. Clim. Res. 43:3-15
15. David, J. R., and P. Capy. 1988. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 4:106-111
16. Deutsch, C. A., J. J. Tewksbury, R. B. Huey, K. S. Sheldon, C. K. Ghalambor, D. C. Haak, et al. 2008. Impacts of climate warming on terrestrial ectotherms across latitude Proc. Natl. Acad. Sci. USA 105:6668-6672
17. Elliott, J. M., J. A. Elliott, and J. D. Allonby. 1994. The critical thermal limits for the stone loach, Noemacheilus barbatulus, from three populations in north-west England. Freshwater Biol. 32:593-601
18. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. Longman Group Limited, Harlow
19. Feder, M. E. 1996. Ecological and evolutionary physiology of stress proteins and the stress response: the Drosophila melanogaster model. Pp. 79-102 in I. A. Johnston and A. F. Bennet, eds. Phenotypic and evolutionary adaptation to temperature. Cambridge Univ. Press, Cambridge
20. Felsenstein, J. 1965. The effect of linkage on directional selection. Genetics 52:349-363
21. Felsenstein, J. 1974. The evolutionary advantage of recombination. Genetics 78:737-756
22. Folk, D. G., P. Zwollo, D. M. Rand, and G. W. Gilchrist. 2006 Selection on knockdown performance in Drosophila melanogaster impacts thermotolerance and heat-shock response differently in females and males. J. Exp. Biol 209:3964-3973
23. Folk, D. G., L. A. Hoekstra, and G. W. Gilchrist. 2007. Critical thermal maxima in knockdown-selected Drosophila: are thermal endpoints correlated? J. Exp. Biol. 210:2649-2656
24. Fraser, A., and D. Burnell. 1970. Computer models in genetics McGraw-Hill, New York
25. Ghalambor, C. K., J. K. McKay, S. P. Carroll, and D. N Reznick. 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21:394-407
26. Gilchrist, G. W., and R. B. Huey. 1999. The direct response of Drosophila melanogaster to selection on knockdown temperature. Heredity 83:15-29
27. González, J., T. L. Karasov, P. W. Messer, and D. A. Petrov 2010. Genome-wide patterns of adaptation to temperate environments associated with transposable elements in Drosophila. PLoS Genet. 6(4):e1000905
28. Hayes, B., and M. E. Goddard. 2001. The distribution of the effects of genes affecting quantitative traits in livestock Genet. Sel. Evol. 33:209-229
29. Helmuth, B., J. G. Kingsolver, and E. Carrington. 2005 Biophysics, physiological ecology, and climate change: does mechanism matter? Ann. Rev. Physiol. 67:177-201
30. Hill, W. G., and A. Robertson. 1966. The effect of linkage on limits to artificial selection. Genet. Res. 8:269-294
31. Hochachka, P. W., and G. N. Somero. 2002. Biochemical adaptation: mechanism and process in physiological evolution. Oxford Univ. Press, New York
32. Hoffmann, A. A. 2010. Physiological climatic limits in Drosophila: patterns and implications. J. Exp. Biol 213:870-880
33. Hoffmann, A. A., and C. M. Sgro. 2011. Climate change and evolutionary adaptation. Nature 470:479-485
34. Hoffmann, A. A., and A. R. Weeks. 2007. Climatic selection on genes and traits after a 100 year-old invasion: a critical look at the temperate-tropical clines in Drosophila melanogaster from eastern Australia. Genetica 129:133-147
35. Hoffmann, A. A., H. Dagher, M. Hercus, and D. Berrigan 1997. Comparing different measures of heat resistance in selected lines of Drosophila melanogaster. J. Insect Physiol 43:393-405
36. Hoffmann, A. A., R. J. Hallas, J. A. Dean, and M. Schiffer 2003a. Low potential for climatic stress adaptation in a rainforest Drosophila species. Science 301:100-102
37. Hoffmann, A. A., J. G. Sørensen, and V. Loeschcke. 2003b Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches. J. Therm Biol 28:175-216
38. Huey, R. B., L. Partridge, and K. Fowler. 1991. Thermal sensitivity of Drosophila melanogaster responds to laboratory natural selection. Evolution 45:751-756
39. Huey, R. B., W. D. Crill, J. G. Kingsolver, and K. E. Weber 1992. A method for rapid measurement of heat or cold resistance of small insects. Funct. Ecol. 6:489-494
40. Huey, R. B., C. A. Deutsch, J. J. Tewksbury, L. J. Vitt, P. E Hertz, H. J. Álvarez Pérez, et al. 2009. Why tropical forest lizards are vulnerable to climate warming. Proc. R. Soc London B 276:1939-1948
41. Jenkins, N. L., and A. A. Hoffmann. 1994. Genetic and maternal variation for heat resistance in Drosophila from the field. Genetics 137:783-789
42. Kellermann, V. M., B. van Heerwaarden, A. A. Hoffmann, and C. M. Sgro'. 2006. Very low additive genetic variance and evolutionary potential in multiple populations of two rainforest Drosophila species. Evolution 60:1104-1108
43. Kellermann, V., B. van Heerwaarden, C. M. Sgro', and A. A. Hoffmann. 2009. Fundamental evolutionary limits in ecological traits drive Drosophila species distributions Science 325:1244-1246
44. Krebs, R. A., and V. Loeschcke. 1997. Estimating heritability in a threshold trait: heat-shock tolerance in Drosophila buzzatii Heredity 79:252-259
45. Levins, R. 1969. Thermal acclimation and heat resistance in Drosophila species. Am. Nat. 103:483-499
46. Loeschcke, V., R. A. Krebs, J. Dahlgaard, and P. Michalak 1997. High temperature stress and the evolution of thermal resistance in Drosophila. Pp. 175-190 in R. Bijlsma and V. Loeschcke, eds. Environmental stress adaptation and evolution. Birkhauser Verlag, Basel
47. Lutterschmidt, W. I., and V. H. Hutchinson. 1997. The critical thermal maximum: data to support the onset of spasms as the definitive end point. Can. J. Zool. 75:1553-1560
48. MathWorks. 2005. MATLAB. Version 7.0.4. MathWorks, Inc., Natick, MA. Available via
49. Maynard Smith, J. 1957. Temperature tolerance and acclimatization in Drosophila subobscura. J. Exp. Biol. 34:85-96
50. McColl, G., A. A. Hoffmann, and S. W. McKechnie. 1996 Response of two heat shock genes to selection for knockdown heat resistance in Drosophila melanogaster Genetics 143:1615-1627
51. Mitchell, K. A., and A. A. Hoffmann. 2010. Thermal ramping rate influences evolutionary potential and species differences for upper thermal limits in Drosophila. Funct. Ecol. 24:694-700
52. Mora, C., and M. F. Maya. 2006. Effect of the rate of temperature increase of the dynamic method on the heat tolerance of fishes. J. Therm. Biol 31:337-341
53. Mousseau, T. A., and D. A. Roff. 1987. Natural selection and the heritability of fitness components. Heredity 59:181-197
54. Orr, H. A. 1999. The evolutionary genetics of adaptation: a simulation study. Genet. Res. 74:207-214
55. Overgaard, J., A. A. Hoffmann, and T. N. Kristensen. 2011a Assesing population and environmental effects on thermal resistance in Drosophila melanogaster using ecologically relevant assays. J. Therm. Biol 36:409-416
56. Overgaard, J., T. N. Kristensen, K. A. Mitchell, and A. A. Hoffmann. 2011b. Thermal tolerance and tropical Drosophila species: does phenotypic plasticity increase with latitude? Am. Nat. 178:S80-S96
57. Parkash, P., V. Sharma, and B. Kalra. 2010. Correlated changes in thermotolerance traits and body color phenotypes in montane populations of Drosophila melanogaster: analysis of within- and between-population variations. J. Zool. 280:49-59
58. Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Evol. Syst. 37:637-669
59. Parsons, P. A. 1980. Parallel climatic races for tolerances to high temperature-desiccation stress in two Drosophila species. J. Biogeog. 7:97-101
60. Peck, L. S., M. S. Clark, S. A. Morley, A. Massey, and H. Rossetti. 2009. Animal temperature limits and ecological relevance: effects of size, activity and rates of change. Funct Ecol. 23:248-256
61. Powell, J. R. 1997. Progress and prospects in evolutionary biology The Drosophila model. Oxford Univ. Press, New York
62. Rako, L., M. J. Blacket, S. W. McKechnie, and A. A Hoffmann. 2007. Candidate genes and thermal phenotypes: identifying ecologically important genetic variation for thermotolerance in the Australian Drosophila melanogaster cline. Mol. Ecol. 16:2948-2957
63. Rand, D. M., D. M. Weinreich, D. Lerman, D. Folk, and G W. Gilchrist. 2010. Three selections are better than one: clinal variation of thermal QTL from independent selection experiments in Drosophila. Evolution 64:2921- 2934
64. Rezende, E. L., and M. Santos. 2012. Comment on 'Ecologically relevant measures of tolerance to potentially lethal temperatures'. J. Exp. Biol. 215:702-703
65. Rezende, E. L., M. Tejedo, and M. Santos. 2011. Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications Funct. Ecol. 25:111-121
66. Ribeiro, P. L., A. Camacho, and C. A. Navas. 2012 Considerations for assessing maximum critical temperatures in small ectothermic animals: insights from leaf-cutting ants PLoS ONE 7:e32083
67. Rockman, M. V. 2012. The QTN program and the alleles that matter for evolution: all that's gold does not glitter Evolution 66:1-17
68. Roff, D. A., and T. A. Mousseau. 1987. Quantitative genetics and fitness: lessons from Drosophila. Heredity 58:103-118
69. Santos, M., L. E. Castañeda, and E. L. Rezende. 2011. Making sense of heat tolerance estimates in ectotherms: lessons from Drosophila. Funct. Ecol. 25:1169-1180
70. Schmidt, P. S., L. Matzkin, M. L. Ippolito, and W. F. Eanes 2005. Geographic variation in diapause incidence, life history traits, and climatic adaptation in Drosophila melanogaster. Evolution 59:1721-1732
71. Sezgin, E., D. D. Duvernell, L. M. Matzkin, Y. Duan, C.-T Zhu, B. C. Verrelli, et al. 2004. Single locus latitudinal clines in metabolic genes, derived alleles, and their relationship to temperate adaptation in Drosophila melanogaster. Genetics 168:923-931
72. Sgró, C. M., J. Overgaard, T. N. Kristensen, K. A. Mitchell, F. E Cockerell, and A. A. Hoffmann. 2010. A comprehensive assessment of geographic variation in heat tolerance and hardening capacity in populations of Drosophila melanogaster from eastern Australia. J. Evol. Biol. 23:2484-2493
73. Shrimpton, A. E., and A. Robertson. 1988. The isolation of polygenic factors controlling bristle score in Drosophila melanogaster. II. Distribution of third chromosome bristle effects within chromosome sections. Genetics 118:445-459
74. Skelly, D. K., L. N. Joseph, H. P. Possingham, L. K Freidenburg, T. J. Farrugia, M. T. Kinnison, et al. 2007 Evolutionary responses to climate change. Cons. Biol 21:1353-1355
75. Sørensen, J. G., M. M. Nielsen, M. Kruhøffer, J. Justesen, and V. Loeschcke. 2005. Full genome gene expression analysis of the heat stress response in Drosophila melanogaster. Cell Stress Chap. 10:312-328
76. Sunday, J. M., A. E. Bates, and N. K. Dulvy. 2011. Global analysis of thermal tolerance and latitude in ectotherms Proc. R. Soc. London B 278:1823-1830
77. Terblanche, J. S., J. A. Deere, S. Clusella-Trullas, C. Janion, and S L. Chown. 2007. Critical thermal limits depend on methodological context. Proc. R. Soc. London B 274:2935-2942
78. Terblanche, J. S., S. Clusella-Trullas, J. A. Deere, and S. L Chown. 2008. Thermal tolerance in a south-east African population of the tsetse fly Glossina pallidipes (Diptera, Glossinidae): implications for forecasting climate change impacts. J. Insect Physiol. 54:114-127
79. Visser, M. E. 2008. Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R. Soc. London B 275:649-659
80. Williams, A. E., M. R. Rose, and T. J. Bradley. 1997. CO2 release patterns in Drosophila melanogaster: the effect of selection for desiccation resistance. J. Exp. Biol. 200:615-624
81. Wolak, M. E., D. J. Fairban, and Y. R. Paulsen. 2011 Guidelines for estimating repeatability. Methods Ecol. Evol 3:129-137