Climate warming and Bergmann's rule through time: Is there any evidence?

Evolutionary Applications

Volumn 7, Issue 1, 2014, Pages 156-168

  Teplitsky, Celine ^a   Millien, Virginie ^b  

^a SORBONNE UNIVERSITÉ   (France)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Adaptation; Animal model; Bergmann's rule; Birds; Body size; Climate change; Mammals; Microevolution; Natural selection; Phenotypic plasticity

Indexed keywords

EID: 84891917693     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12129     Document Type: Article

References (109)

1. Allen, J. A. 1877. The influence of physical conditions in the genesis of species. Radical Review 1:108-140.
2. Andersson, M. 1994. Sexual Selection. Princeton University Press, Princeton, NJ.
3. Arnold, S. J., M. E. Pfrender, and A. G. Jones 2001. The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112:9-32.
4. Ashton, K. G. 2002. Patterns of within-species body size variation of birds: strong evidence for Bergmann's rule. Global Ecology and Biogeography 11:505-523.
5. Ashton, K. G., M. C. Tracy, and A. de Queiroz 2000. Is Bergmann's rule valid for mammals? American Naturalist 156:390-415.
6. Barnett, S. A., and R. G. Dickson 1984. Changes among wild House mice (Mus musculus) bred for ten generations in a cold environment, and their evolutionary implications. Journal of Zoology 203:163-180.
7. Bergmann, C. 1847. Ueber die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Gottinger Studien 3:595-708.
8. Berteaux, D., D. Reale, A. G. McAdam, and S. Boutin 2004. Keeping pace with fast climate change: Can arctic life count on evolution? Integrative and Comparative Biology 44:140-151.
9. Berteaux, D., M. M. Humphries, C. J. Krebs, M. Lima, A. G. McAdam, N. Pettorelli, D. Réale et al. 2006. Constraints to projecting the effects of climate change on mammals. Climate Research 32:151-158.
10. Blackburn, T. M., K. J. Gaston, and N. Loder 1999. Geographic gradients in body size: a clarification of Bergmann's rule. Diversity and Distributions 5:165-174.
11. Blois, J. L., R. S. Feranec, and E. A. Hadly 2008. Environmental influences on spatial and temporal patterns of body-size variation in California ground squirrels (Spermophilus beecheyi). Journal of Biogeography 35:602-613.
12. Boutin, S., and J. E. Lane 2014. Climate change and mammals: evolutionary versus plastic responses. Evolutionary Applications 7:29-41.
13. Bradshaw, W. E., and C. M. Holzapfel 2006. Evolutionary response to rapid climate change. Science 312:1477-1478.
14. Brown, C. R., M. B. Brown, and E. A. Roche 2013. Fluctuating viability selection on morphology of cliff swallows is driven by climate. Journal of Evolutionary Biology 26:1129-1142.
15. Carroll, S. P., A. P. Hendry, D. N. Reznick, and C. W. Fox 2007. Evolution on ecological time-scales. Functional Ecology 21:387-393.
16. Charmantier, A., and P. Gienapp 2014. Climate change and timing of avian breeding and migration: evolutionary versus plastic changes. Evolutionary Applications 7:15-28.
17. Charmantier, A., R. H. McCleery, L. R. Cole, C. Perrins, L. E. B. Kruuk, and B. C. Sheldon 2008. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320:800-803.
18. Chevin, L.-M., S. Collins, and F. Lefèvre 2013. Phenotypic plasticity and evolutionary demographic responses to climate change: taking theory out to the field. Functional Ecology. 27:966-979.
19. Chown, S. L., A. A. Hoffmann, T. N. Kristensen, M. J. J. Angilletta, N. C. Stenseth, and C. Pertoldi 2010. Adapting to climate change: a perspective from evolutionary physiology. Climate Research 43:3-15.
20. Clutton-Brock, T., and B. C. Sheldon 2010. Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends in Ecology & Evolution 25:562-573.
21. Coltman, D. W., P. O'Donoghue, J. T. Jorgenson, J. T. Hogg, C. Strobeck, and M. Festa-Bianchet 2003. Undesirable evolutionary consequences of trophy hunting. Nature 426:655-658.
22. Coulson, T., and S. Tuljapurkar 2008. The dynamics of a quantitative trait in an age-structured population living in a variable environment. American Naturalist 172:599-612.
23. Cushman, J. H., J. H. Lawton, and F. J. Manly 1993. Latitudinal patterns in European ant assemblages: Variation in species richness and body size. Oecologia 95:30-37.
24. Damuth, J., and B. J. McFadden 1990. Body Size in Mammalian Paleobiology. Estimation and Biological Implications. Cambridge University Press, Cambridge.
25. Eastman, L. M., T. L. Morelli, K. C. Rowe, C. J. Conroy, and C. Moritz 2012. Size increase in high elevation ground squirrels over the last century. Global Change Biology 18:1499-1508.
26. Gardner, J. L., R. Heinsohn, and L. Joseph 2009. Shifting latitudinal clines in avian body size correlate with global warming in Australian passerines. Proceedings of the Royal Society B-Biological Sciences 276:3845-3852.
27. Gardner, J. L., A. Peters, M. Kearney, L. Joseph, and R. Heinsohn 2011. Declining body size: a third universal response to warming? Trends in Ecology & Evolution 26:285-291.
28. 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. Functional Ecology 21:394-407.
29. Gienapp, P., C. Teplitsky, J. S. Alho, J. A. Mills, and J. Merilä 2008. Climate change and evolution: disentangling environmental and genetic responses. Molecular Ecology 17:167-178.
30. Goodman, R. E., G. Lebuhn, N. E. Seavy, T. Gardali, and J. D. Bluso-Demers 2012. Avian body size changes and climate change: warming or increasing variability? Global Change Biology 18:63-73.
31. Gould, S. J., and R. C. Lewontin 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proceedings of the Royal Society of London (B) 205:581-598.
32. Grant, P. R., and B. R. Grant 2002. Unpredictable evolution in a 30-year study of Darwin's finches. Science 296:707-711.
33. Grant, B. R., and P. R. Grant 2003. What Darwin's finches can teach us about the evolutionary origin and regulation of biodiversity. BioScience 53:965-975.
34. Gratten, J., A. J. Wilson, A. F. McRae, D. Beraldi, P. M. Visscher, J. Pemberton, and J. Slate 2010. No evidence for warming climate theory of coat colour change in Soay sheep: a comment on Maloney et al. Biology Letters 6:678-679.
35. Hadfield, J. D. 2010. MCMC methods for multi-response generalised linear mixed models: The MCMCglmm R package. Journal of Statistical Software 33:1-22.
36. Hadfield, J. D., A. J. Wilson, D. Garant, B. C. Sheldon, and L. E. B. Kruuk 2010. The misuse of BLUP in ecology and evolution. American Naturalist 175:116-125.
37. Hairston, N. G., S. P. Ellner, M. A. Geber, T. Yoshida, and J. A. Fox 2005. Rapid evolution and the convergence of ecological and evolutionary time. Ecology Letters 8:1114-1127.
38. Hansen, M. M., I. Olivieri, D. M. Waller, and E. E. Nielsen, and The GeM Working Group 2012. Monitoring adaptive genetic responses to environmental change. Molecular Ecology 21:1311-1329.
39. Hendry, A. P., and M. T. Kinnison 2001. An introduction to microevolution: rate, pattern, process. Genetica 112-113:1-8.
40. Hendry, A. P., T. J. Farrugia, and M. T. Kinnison 2008. Human influences on rates of phenotypic change in wild animal populations. Molecular Ecology 17:20-29.
41. Ho, C.-K., S. C. Pennings, and T. H. Carefoot 2010. Is diet quality an overlooked mechanism for Bergmann's rule? American Naturalist 175:269-276.
42. Hoffmann, A. A., and Y. Willi 2008. Detecting genetic responses to environmental change. Nature Reviews - Genetics 9:421-432.
43. Husby, A., S. M. Hille, and M. E. Visser 2011. Testing mechanisms of Bergmann's rule: phenotypic decline but no genetic change in body size in three Passerine bird populations. American Naturalist 178:202-213.
44. Jiguet, F., R. Julliard, C. D. Thomas, O. Dehorter, S. E. Newson, and D. Couvet 2006. Thermal range predicts bird population resilience to extreme high temperatures. Ecology Letters 9:1321-1330.
45. de Jong, G. 2005. Evolution of phenotypic plasticity: patterns of plasticity and the emergence of ecotypes. New Phytologist 166:101-118.
46. Kerr, J. T., and S. Z. Dobrowski 2013. Predicting the impacts of global change on species, communities and ecosystems: it takes time. Global Ecology and Biogeography 22:261-263.
47. Kingsolver, J. G., S. E. Diamond, A. M. Siepielski, and S. M. Carlson 2012. Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evolutionary Ecology 26:1101-1118.
48. Koontz, T. L., U. L. Shepherd, and D. Marshall 2001. The effects of climate change on Merriam's kangaroo rat, Dipodomys merriami. Journal of Arid Environments 49:581-591.
49. Kopp, M., and S. Matuszewski 2014. Rapid evolution of quantitative traits: theoretical perspectives. Evolutionary Applications 7:169-191.
50. Kovach-Orr, C., and G. F. Fussmann 2013. Evolutionary and plastic rescue in multitrophic model communities. Philosophical Transactions of the Royal Society of London B 368:20120084.
51. Kruuk, L. E. B. 2004. Estimating genetic parameters in natural populations using the 'animal model'. Philosophical Transactions of the Royal Society of London (B) 359:873-890.
52. Lande, R., and S. J. Arnold 1983. The measurement of selection on correlated characters. Evolution 37:1210-1226.
53. Marroig, G., and J. Cheverud 2010. Size as a line of least resistance II: Direct selection on size or correlated response due to constraints? Evolution 64:1470-1488.
54. Mayr, E. 1956. Geographical character gradients and climatic adaptation. Evolution 10:105-108.
55. McCoy, D. E. 2012. Connecticut birds and climate Change: Bergmann's rule in the fourth dimension. Northeastern Naturalist 19:323-334.
56. McKechnie, A. E., and B. O. Wolf 2010. Climate change increases the likelihood of catastrophic avian mortality events during extreme heat waves. Biology Letters 6:253-256.
57. McNab, B. K. 2010. Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164:13-23.
58. Meiri, S. 2011. Bergmann's Rule - what's in a name? Global Ecology and Biogeography 20:203-207.
59. Meiri, S., and T. Dayan 2003. On the validity of Bergmann's rule. Journal of Biogeography 30:331-351.
60. Meiri, S., D. Guy, T. Dayan, and D. Simberloff 2009. Global change and carnivore body size: data are stasis. Global Ecology and Biogeography 18:240-247.
61. Merilä, J., and A. P. Hendry 2014. Climate change, adaptation and phenotypic plasticity: the problem and the evidence. Evolutionary Applications 7:1-14.
62. Merilä, J., L. E. B. Kruuk, and B. C. Sheldon 2001a. Cryptic evolution in a wild bird population. Nature 412:76-79.
63. Merilä, J., B. C. Sheldon, and L. E. B. Kruuk 2001b. Explaining stasis: microevolutionary studies in natural populations. Genetica 112:199-222.
64. Millien, V., S. K. Lyons, L. Olson, F. A. Smith, A. B. Wilson, and Y. Yom-Tov 2006. Ecotypic variation in the context of global climate change: revisiting the rules. Ecology Letters 9:853-869.
65. Moreno-Rueda, G., and J. M. Rivas 2007. Recent changes in allometric relationships among morphological traits in the dipper (Cinclus cinclus). Journal of Ornithology 148:489-494.
66. Morrissey, M. B., and J. D. Hadfield 2012. Directional selection in temporally replicated studies is remarkably consistent. Evolution 66:435-442.
67. Morrissey, M. B., L. E. B. Kruuk, and A. J. Wilson 2010. The danger of applying the breeder's equation in observational studies of natural populations. Journal of Evolutionary Biology 23:2277-2288.
68. Olalla-Tarraga, M. A. 2011. "Nullius in Bergmann" or the pluralistic approach to ecogeographical rules: a reply to Watt et al. (2010). Oikos 120:1441-1444.
69. Olson, V. A., R. G. Davies, C. D. L. Orme, G. H. Thomas, S. Meiri, T. M. Blackburn, K. J. Gaston et al. 2009. Global biogeography and ecology of body size in birds. Ecology Letters 12:249-259.
70. Ozgul, A., S. Tuljapurkar, T. G. Benton, J. M. Pemberton, T. H. Clutton-Brock, and T. Coulson 2009. The dynamics of phenotypic change and the shrinking sheep of St. Kilda. Science 325:464-467.
71. Ozgul, A., D. Z. Childs, M. K. Oli, K. B. Armitage, D. T. Blumstein, L. E. Olson, S. Tuljapurkar et al. 2010. Coupled dynamics of body mass and population growth in response to environmental change. Nature 466:482-485.
72. Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annual Review of Ecology Evolution and Systematics 37:637-669.
73. Parmesan, C., and G. Yohe 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37-42.
74. Phillimore, A. B., J. D. Hadfield, O. R. Jones, and R. J. Smithers 2010. Differences in spawning date between populations of common frog reveal local adaptation. Proceedings of the National Academy of Sciences of the United States of America 107:8292-8297.
75. Polly, P. D., J. T. Eronen, M. Fred, G. P. Dietl, V. Mosbrugger, C. Scheidegger, D. C. Frank et al. 2011. History matters: ecometrics and integrative climate change biology. Proceedings of the Royal Society B: Biological Sciences 278:1131-1140.
76. Post, E., R. Langvatn, M. C. Forchhammer, and N. C. Stenseth 1999. Environmental variation shapes sexual dimorphism in red deer. Proceedings of the National Academy of Sciences of the United States of America 96:4467-4471.
77. Postma, E. 2006. Implications of the difference between true and predicted breeding values for study of natural selection and micro-evolution. Journal of Evolutionary Biology 19:309-320.
78. Postma, E., and A. Charmantier 2007. What 'animal models' can and cannot tell ornithologists about the genetics of wild populations. Journal of Ornithology 148:S633-S642.
79. Price, G. 1970. Selection and covariance. Nature 227:520-521.
80. Price, T., and T. Langen 1992. Evolution of correlated characters. Trends in Ecology & Evolution 7:307-310.
81. Price, T., M. Kirkpatrick, and S. J. Arnold 1988. Directional selection and the evolution of breeding date in birds. Science 240:798-799.
82. Riek, A., and F. Geiser 2012. Developmental phenotypic plasticity in a marsupial. Journal of Experimental Biology 215:1552-1558.
83. Rode, K. D., S. C. Amstrup, and E. V. Regehr 2010. Reduced body size and cub recruitment in polar bears associated with sea ice decline. Ecological Applications 20:768-782.
84. Root, T. L., J. T. Price, K. R. Hall, S. H. Schneider, C. Rosenzweig, and J. A. Pounds 2003. Fingerprints of global warming on wild animals and plants. Nature 421:57-60.
85. Sheridan, J. A., and D. Bickford 2011. Shrinking body size as an ecological response to climate change. Nature Climate Change 1:401-406.
86. Siepielski, A. M., J. D. DiBattista, and S. M. Carlson 2009. It's about time: the temporal dynamics of phenotypic selection in the wild. Ecology Letters 12:1261-1276.
87. Smith, F. A., L. Betancourt, and J. H. Brown 1995. Evolution of body size in the woodrat over the past 25, 000 years of climate change. Science 270:2012-2014.
88. Stenseth, N. C., A. Mysterud, G. Ottersen, J. W. Hurrell, K. S. Chan, and M. Lima 2002. Ecological effects of climate fluctuations. Science 297:1292-1296.
89. Stillwell, R. C. 2010. Are latitudinal clines in body size adaptive? Oikos 119:1387-1390.
90. Teplitsky, C., J. A. Mills, J. S. Alho, J. W. Yarrall, and J. Merilä 2008. Bergmann's rule and climate change revisited: Disentangling environmental and genetic responses in a wild bird population. Proceedings of the National Academy of Sciences of the United States of America 105:13492-13496.
91. Thompson, J. N. 1998. Rapid evolution as an ecological process. Trends in Ecology and Evolution 13:329-332.
92. Urban, M. C., and B. Phillips 2014. Plasticity and genetic adaptation mediate amphibian and reptile responses to climate change. Evolutionary Applications 7:88-103.
93. Van Buskirk, J., R. S. Mulvihill, and R. C. Leberman 2010. Declining body sizes in North American birds associated with climate change. Oikos 119:1047-1055.
94. Van de Pol, M., and J. Wright 2009. A simple method for distinguishing within- versus between-subject effects using mixed models. Animal Behavior 77:753-758.
95. Walsh, B., and M. W. Blows 2009. Abundant genetic variation plus strong selection = Multivariate genetic constraints: A geometric view of adaptation. Annual Review of Ecology Evolution and Systematics 40:41-59.
96. Walther, G. R., E. Post, P. Convey, A. Menzel, C. Parmesan, T. J. C. Beebee, J. M. Fromentin et al. 2002. Ecological responses to recent climate change. Nature 416:389-395.
97. Watt, C., and V. Salewski 2011. Bergmann's rule encompasses mechanism: a reply to Olalla-Tarraga (2011). Oikos 120:1445-1447.
98. Wilson, A. J., J. M. Pemberton, J. G. Pilkington, T. H. Clutton-Brock, D. W. Coltman, and L. E. B. Kruuk 2007. Quantitative genetics of growth and cryptic evolution of body size in an island population. Evolutionary Ecology 21:337-356.
99. Wilson, A. J., D. Reale, M. N. Clements, M. M. Morrissey, E. Postma, C. A. Walling, L. E. B. Kruuk et al. 2010. An ecologist's guide to the animal model. Journal of Animal Ecology 79:13-26.
100. Yom-Tov, Y. 2001. Global warming and body mass decline in Israeli passerine birds. Proceedings of the Royal Society of London (B) 268:947-952.
101. Yom-Tov, Y., and E. Geffen 2011. Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls. Biological Reviews 86:531-541.
102. Yom-Tov, Y., and J. Yom-Tov 2005. Global warming, Bergmann's rule and body size in the masked shrew Sorex cinereus Kerr in Alaska. Journal of Animal Ecology 74:803-808.
103. Yom-Tov, Y., Y. Benjamini, and S. Kark 2002. Global warming, Bergmann's rule and body mass - are they related? The chukar partridge (Alectoris chukar) case. Journal of Zoology 257:449-455.
104. Yom-Tov, Y., S. Yom-Tov, and H. Baagoe 2003. Increase of skull size in the red fox (Vulpes vulpes) and Eurasian badger (Meles meles) in Denmark during the twentieth century: an effect of improved diet? Evolutionary Ecology Research 5:1037-1048.
105. Yom-Tov, Y., T. M. Heggberget, O. Wiig, and S. Yom-Tov 2006a. Body size changes among otters, Lutra lutra, in Norway: the possible effects of food availability and global warming. Oecologia 150:155-160.
106. Yom-Tov, Y., S. Yom-Tov, J. Wright, C. J. R. Thorne, and R. Du Feu 2006b. Recent changes in body weight and wing length among some British passerine birds. Oikos 112:91-101.
107. Yom-Tov, Y., S. Yom-Tov, and G. Jarrell 2008. Recent increase in body size of the American marten Martes americana in Alaska. Biological Journal of the Linnean Society 93:701-707.
108. Yom-Tov, Y., N. Leader, S. Yom-Tov, and H. J. Baagoe 2010a. Temperature trends and recent decline in body size of the stone marten Martes foina in Denmark. Mammalian Biology 75:146-150.
109. Yom-Tov, Y., A. Roos, P. Mortensen, O. Wiig, S. Yom-Tov, and T. M. Heggberget 2010b. Recent changes in body size of the Eurasian otter Lutra lutra in Sweden. Ambio 39:496-503.