Thermal adaptation in endotherms: Climate and phylogeny interact to determine population-level responses in a wild rat

Functional Ecology

Volumn 26, Issue 2, 2012, Pages 390-398

  Glanville, Elsa J ^a   Murray, Shauna A ^b   Seebacher, Frank ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Body temperature; Brown adipose tissue; Climate change; Energetics; Gene environment interaction; Mitochondria; Thermal ecology; Thermoregulation; Uncoupling protein 1

Indexed keywords

ADAPTATION; BIOENERGETICS; BODY TEMPERATURE; CLIMATE CHANGE; COLD TOLERANCE; ECOPHYSIOLOGY; ENDOTHERMY; GENOTYPE-ENVIRONMENT INTERACTION; MITOCHONDRION; MORPHOLOGY; PHYLOGENETICS; PHYLOGENY; PROTEIN; RELATEDNESS; RODENT; TEMPERATURE EFFECT; THERMAL EVOLUTION;

AVES; MAMMALIA; RATTUS; RATTUS FUSCIPES;

EID: 84859104755     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2011.01933.x     Document Type: Article

References (66)

1. Acin-Perez, R., Gatti, D.L., Bai, Y. & Manfredi, G. (2011) Protein phosphorylation and prevention of cytochrome oxidase inhibition by ATP: coupled mechanisms of energy metabolism regulation. Cell Metabolism, 13, 712-719.
2. Aljanabi, S. & Martinez, I. (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR- based techniques. Nucleic Acids Research, 25, 4692-4693.
3. Amo, T. & Brand, M.D. (2007) Were inefficient mitochondrial haplogroups selected during migrations of modern humans? A test using modular kinetic analysis of coupling in mitochondria from cybrid cell lines. Biochemical Journal, 404, 345-351.
4. Amo, T., Yadava, N., Oh, R., Nicholls, D.G. & Brand, M.D. (2008) Experimental assessment of bioenergetic differences caused by the common European mitochondrial DNA haplogroups H and T. Gene, 411, 69-76.
5. Ballard, J.W.O., Melvin, R.G., Katewa, S.D. & Maas, K. (2008) Mitochondrial DNA variation is associated with measurable differences in life-history traits and mitochondrial metabolism in Drosophila simulans. Evolution, 61, 1735-1747.
6. Belevich, I., Bloch, D.A., Belevich, N., Wikström, M. & Verkhovsky, M.I. (2007) Exploring the proton pumping mechanism of cytochrome c oxidase. Proceedings of the National Academy of Sciences USA, 104, 2685-2690.
7. Blaake, E.E., Vanbaak, M.A., Kempen, K.P.S. & Saris, W.H.M. (1993) Role of alpha-adrenoceptors and beta-adrenoceptors in sympathetically mediated thermogenesis. American Journal of Physiology, 264, E11-E17.
8. Bland, M.L. & Birnbaum, M.J. (2011) ADaPting to energetic stress. Science, 332, 1387.
9. Böckler, H., Steinlechner, S. & Heldmaier, G. (1982) Complete cold substitution of noradrenaline-induced thermogenesis in the Djungarian hamster, Phodopus sungorus. Experientia, 38, 261-262.
10. 4-adrenergic receptor on the expression of uncoupling proteins and peroxisome proliferator-activated receptor-γ coactivator -1. Biochemical and Biophysical Research Communications, 261, 8170-8876.
11. Bozinovic, F. & Rosenmann, M. (1989) Maximum metabolic rate of rodents: physiological and ecological consequences on distributional limits. Functional Ecology, 3, 173-181.
12. Bremer, K. & Moyes, C.D. (2011) Origins of variation in muscle cytochrome c oxidase activity within and between fish species. Journal of Experimental Biology, 214, 1888-1895.
13. Burger, R. & Lynch, M. (1995) Evolution and extinction in a changing environment: a quantitative-genetic analysis. Evolution, 49, 151-163.
14. Cannon, B. & Nedergaard, J. (2004) Brown adipose tissue: function and physiological significance. Physiological Reviews, 84, 277-359.
15. Caterina, M.J. (2007) Transient receptor potential ion channels as participants in thermosensation and thermoregulation. American Journal of Physiology Regulatory, Integrative and Comparative Physiology, 292, R64-R76.
16. Chown, S.L., Hoffmann, A.A., Kristensen, T.N., Angilletta, M.J. Jr, Stenseth, N.C. & Pertoldi, C. (2010) Adapting to climate change: a perspective from evolutionary physiology. Climate Research, 43, 3-15.
17. Duteil, D., Chambon, C., Ali, F., Malivindi, R., Zoll, J., Kato, S., Geny, B., Chambon, P. & Metzger, D. (2010) The transcriptional coregulators TIF2 and SRC-1 regulate energy homeostasis by modulating mitochondrial respiration in skeletal muscles. Cell Metabolism, 12, 496-508.
18. Felsenstein, J. (1985) Phylogenies and the comparative method. The American Naturalist, 125, 1-15.
19. Fukuoh, A. & Kang, D. (2009) Methods for assessing binding of mitochondrial transcription factor A (TFAM) to DNA. Mitochondrial DNA: Methods and Protocols, 554, 87-101.
20. Geiser, F. (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Annual Review of Physiology, 66, 239-274.
21. Glanville, E.J. & Seebacher, F. (2010) Plasticity in body temperature and metabolic capacity sustain winter activity in a small endotherm (Rattus fuscipes). Comparative Biochemistry and Physiology A, 155, 383-391.
22. Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696-704.
23. Hardie, D.G. (2008) Role of AMP-activated protein kinase in the metabolic syndrome and in heart disease. FEBS Letters, 582, 81-89.
24. Harte, J., Ostling, A., Green, J.L. & Kinzig, A. (2004) Biodiversity conservation: climate change and extinction risk. Nature, 430, doi:
25. Heldmaier, G. (1989) Seasonal acclimatization of energy requirements in mammals: functional significance of body weight control, hypothermia, torpor and hibernation. Energy Transformation in Cells and Organisms (eds W. Wieser & E. Gaigner ), pp. 130-139. Georg Thieme Verlag, Stuttgart.
26. Herzig, S., Long, S., Jhala, U.S., Hendrick, S., Quinn, R., Bauer, A., Rudolph, D., Schutz, G., Yoon, C., Puigserver, P., Spiegelman, B. & Montminy, M. (2001) CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature, 413, 179-183.
27. Huelsenbeck, J.P. & Ronquist, F. (2001) Mr. Bayes: Bayesian inference of phylogeny. Bioinformatics, 17, 754-755.
28. Intergovernmental Panel of Climate Change. (2007) Climate Change 2007: Impacts, Adaptation and Vulnerability. Cambridge University Press, Cambridge.
29. Irrcher, I., Ljubicic, V., Kirwan, A.F. & Hood, D.A. (2008) AMO-activated protein kinase-regulated activation of the PGC-1α promoter in skeletal muscle cells. PLoS ONE, 3, e3614.
30. Johnson, H.E., Lloyd, A.J., Muir, L.A.J., Smith, A.R. & Causton, D.R. (2007) The application of MANOVA to analyse Arabidopsis thaliana metabolomic data from factorially designed experiments. Metabolomics, 3, 517-530.
31. Koch, L.G. & Britton, S.L. (2007) Aerobic metabolism underlies complexity and capacity. Journal of Physiology, 586, 83-95.
32. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J. & Higgins, D.G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
33. LeMoine, C.M.R., Lougheed, S.C. & Moyes, C.D. (2010) Modular evolution of PGC-1α in vertebrates. Journal of Molecular Evolution, 70, 492-505.
34. Lin, J., Handschirm, C. & Spiegelman, B.M. (2005) Metabolic control through the PGC-1 family of transcription coactivators. Cell Metabolism, 1, 361-370.
35. Little, A.G., Kocha, K.M., Lougheed, S.C. & Moyes, C.D. (2010a) Evolution of the nuclear-encoded cytochrome oxidase subunits in vertebrates. Physiological Genomics, 42, 76-84.
36. Little, J.P., Safdar, A., Cermak, N., Tarnopolsky, M.A. & Gibala, M.J. (2010b) Acute endurance exercise increases the nuclear abundance of PGC-1α in trained human skeletal muscle. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 298, R912-R917.
37. Lowell, B.B. & Spiegelman, B.M. (2000) Towards a molecular understanding of adaptive thermogenesis. Nature, 404, 652-660.
38. McKechnie, A.E. (2008) Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. Journal of Comparative Physiology B, 178, 235-247.
39. Morrison, S.F., Nakamura, K. & Madden, C.J. (2008) Central control of thermogenesis in mammals. Experimental Physiology, 93, 773-797.
40. Moyes, C.D. (2003) Controlling muscle mitochondrial content. Journal of Experimental Biology, 206, 4385-4391.
41. Nagy, K.A. (2005) Field metabolic rate and body size. Journal of Experimental Biology, 208, 1621-1625.
42. Nakamura, K., Matsumura, K., Hübschle, T., Nakamura, Y., Hioki, H., Fujiyama, F., Boldogköi, Z., König, M., Thiel, H.-J., Gerstberger, R., Kobayashi, S. & Kaneko, T. (2004) Identification of sympathetic premotor neurons in medullary raphe regions mediating fever and other thermoregulatory functions. Journal of Neuroscience, 24, 5370-5380.
43. Nespolo, R.F., Bacigalupe, L.D. & Bozinovic, F. (2003) Heritability of energetics in a wild mammal, the leaf-eared mouse (Phyllotis darwini). Evolution, 57, 1679-1688.
44. Nespolo, R.F., Verdugo, C., Cortes, P.A. & Bacigalupe, L.D. (2010) Bioenergetics of torpor in the Microbiotherid marsupial, Monito del Monte (Dromiciops gliroides): the role of temperature and food availability. Journal of Comparative Physiology B, 180, 767-773.
45. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 29, e45.
46. Porter, W.P. & Kearney, M. (2009) Size, shape, and the thermal niche of endotherms. Proceedings of the National Academy of Science USA, 106(Suppl. 2), 19666-19672.
47. Puigserver, P., Wu, Z., Park, C.W., Graves, R., Wright, M. & Spiegelman, B.M. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell, 92, 829-839.
48. Quinn, G. & Keough, M. (2004) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge.
49. Reynolds, P.S. (1993) Effects of body size and fur on heat loss of collared lemmings, Dicrostonyx groenlandicus. Journal of Mammalogy, 74, 291-303.
50. Robins, J.H., Hingston, M., Matisoo-Smith, E. & Ross, H.A. (2007) Identifying Rattus species using mitochondrial DNA. Molecular Ecology Notes, 7, 717-729.
51. Rodgers, J.T., Lerin, C., Gerhart-Hines, Z. & Puigserver, P. (2008) Metabolic adaptations through PGC-1α and SIRT1 pathways. FEBS Letters, 582, 46-53.
52. Sbisà, E., Tanzariello, F., Reyes, A., Pesole, G. & Saccone, C. (1997) Mammalian mitochondrial D-loop region structural analysis: identification of new conserved sequences and their functional and evolutionary implications. Gene, 205, 125-140.
53. Scarpulla, R.C. (2008) Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiological Reviews, 88, 611-638.
54. Sears, M.W., Hayes, J.P., Banta, M.R. & McCormick, D. (2009) Out in the cold: physiological capacity influences behaviour in deer mice. Functional Ecology, 23, 774-783.
55. Seebacher, F. & Glanville, E.J. (2010) Low levels of physical activity increase metabolic responsiveness to cold in a rat (Rattus fuscipes). PLoS ONE, 5, e13022.
56. Seebacher, F., Murray, S.A. & Else, P.L. (2009) Thermal acclimation and regulation of metabolism in a reptile (Crocodylus porosus): the importance of transcriptional mechanisms and membrane composition. Physiological and Biochemical Zoology, 82, 766-775.
57. Seebacher, F., Guderley, H., Elsey, R.M. & Trosclair III, P.L. (2003) Seasonal acclimatisation of muscle metabolic enzymes in a reptile (Alligator mississippiensis). Journal of Experimental Biology, 206, 1193-1200.
58. Seebacher, F., Brand, M.D., Else, P.L., Guderley, H., Hulbert, A.J. & Moyes, C.D. (2010) Plasticity of oxidative metabolism in variable climates: molecular mechanisms. Physiological and Biochemical Zoology, 83, 721-732.
59. Tao, N., Richardson, R., Bruno, W. & Kuiken, C. (2005) FindModel.
60. Taylor, M. & Calaby, J.H. (1988) Rattus fuscipes. Mammalian Species, 298, 1-8.
61. Thomas, C.D., Cameron, A., Green, R.E., Bakkenes, M., Beaumont, L.J., Collingham, Y.C., Erasmus, B.F.N., de Siqueira, M.F., Grainger, A., Hannah, L., Hughes, L., Huntley, B., van Jaarsveld, A.S., Midgley, G.F., Miles, L., Ortega-Huerta, M.A., Peterson, A.T., Phillips, O.L. & Williams, S.E. (2004) Extinction risk from climate change. Nature, 427, 145-148.
62. Vazquez-Dominguez, E., Paetkau, D., Tucker, N., Hinten, G. & Moritz, C. (2001) Resolution of natural groups using iterative assignment tests: an example from two species of Australian native rats (Rattus). Molecular Ecology, 10, 2069-2078.
63. Walter, I., Hegarty, B. & Seebacher, F. (2010) AMP-activated protein kinase controls metabolism and heat production during embryonic development in birds. Journal of Experimental Biology, 213, 3167-3176.
64. Warne, R.W., Pershall, A.D. & Wolf, B.O. (2010) Linking precipitation and C-3-C-4 plant productivity to resource dynamics in higher-trophic-level consumers. Ecology, 91, 1628-1638.
65. Wilson, R.S. & Franklin, C.E. (2002) Testing the beneficial acclimation hypothesis. Trends in Ecology and Evolution, 17, 66-70.
66. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R.C. & Spiegelman, B.M. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell, 98, 115-124.