Determinants of intra-specific variation in basal metabolic rate

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 183, Issue 1, 2013, Pages 27-41

  Konarzewski, Marek ^a   Książek, Aneta ^a  

^a UNIVERSITY OF BIALYSTOK   (Poland)

Author keywords

Artificial selection; BMR; Genomics; Intra specific variation; mTOR; Quantitative genetics

Indexed keywords

ANIMALIA; MAMMALIA;

EID: 84871904500     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-012-0698-z     Document Type: Review

References (150)

1. Babik W, Stuglik M, Weihong Q, Kuenzli M, Kuduk K, Koteja P, Radwan J (2010) Heart transcriptome of the bank vole (Myodes glareolus): towards understanding the evolutionary variation in metabolic rate. BMC Genomics 11: 390.
2. Bacigalupe LD, Nespolo RF, Bustamante DM, Bozinovic F (2004) The quantitative genetics of sustained energy budget in a wild mouse. Evolution 58: 421-429.
3. Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206: 649-653.
4. Brze{ogonek}k P, Bielawska K, Ksia{ogonek}żek A, Konarzewski M (2007) Anatomic and molecular correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol Biochem Zool 80: 401-499.
5. Brze{ogonek}k P, Ksia{ogonek}żek A, Dobrzyń A, Konarzewski M (2012) Effect of dietary restriction on metabolic, anatomic and molecular traits in mice depends on the initial level of basal metabolic rate (BMR). J Exp Biol. doi: 10. 1242/jeb. 065318.
6. Bunger L, MacLeod MG, Wallace CA, Hill WG (1998) Direct and correlated effects of selection for food intake corrected for body weight in the adult mouse. In: Proc 6th World Congr Genet Appl Livest Prod, The University of New England, Armidale, Australia pp 97-100.
7. Burton T, Killen SS, Armstrong JD, Metcalfe NB (2011) What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc B 278: 3465-3473.
8. 2max. Physiol Genomics 35: 213-221.
9. Bye A, Langaas M, Höydal MA, Kemi OJ, Heinrich G, Koch LG, Britton SL, Najjar SM, Ellingsen Ø, Wisløff U (2008b) Aerobic capacity-dependent differences in cardiac gene expression. Physiol Genomics 33: 100-109.
10. Cannon B, Nedergaard J (2010) Metabolic consequences of the presence or absence of the thermogenic capacity of brown adipose tissue in mice (and probably in humans). Int J Obes 34: S7-S16.
11. Chappell MA, Garland T Jr, Robertson GF, Saltzman W (2007) Relationships among running performance, aerobic physiology, and organ mass in male Mongolian gerbils. J Exp Biol 210: 4179-4197.
12. Coltman DW (2005) Testing marker-based estimates of heritability in the wild. Mol Ecol 14: 2593-2599.
13. Dohm MR, Hayes JP, Garland T Jr (2001) The quantitative genetics of maximal and basal rates of oxygen consumption in mice. Genetics 159: 267-277.
14. Dulloo AG, Samec S (2001) Uncoupling proteins: their roles in adaptive thermogenesis and substrate metabolism reconsidered. Brit J Nutr 86: 123-139.
15. Duncan AW, Taylor MH, Hickey RD, Hanlon Newell AE, Lenzi ML, Olson SB, Finegold MJ, Grompe M (2010) The ploidy conveyor of mature hepatocytes as a source of genetic variation. Nature 467: 707-710.
16. Elia M (1992) Organ and tissue contribution to metabolic rate. In: Kinney JM, Tucker HN (eds) Energy metabolism: tissue determinants and cellular corollaries. Raven, New York, pp 61-79.
17. Else PL, Wu BJ (1999) What role for membranes in determining the higher sodium pump molecular activity of mammals compared to ectotherms? J Comp Physiol B 169: 296-302.
18. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Essex.
19. Feder ME, Garland T Jr, Marden JH, Zera AJ (2010) Locomotion in response to shifting climate zones: not so fast. Ann Rev of Physiol 72: 167-190.
20. Garant D, Kruuk LEB (2005) How to use molecular marker data to measure evolutionary parameters in wild populations. Mol Ecol 14: 1843-1859.
21. Garland T Jr (2003) Selection experiments: an under-utilized tool in biomechanics and organismal biology. In: Bels VL, Gasc JP, Casinos A (eds) Vertebrate biomechanics and evolution. BIOS, Oxford, pp 23-56.
22. Garland T Jr, Adolph SC (1994) Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol Zool 67: 797-828.
23. Garland T Jr, Midford PE, Ives AR (1999) An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Am Zool 39: 374-388.
24. Garland T Jr, Morgan MT, Swallow JG, Rhodes JS, Girard I, Belter JG, Carter PA (2002) Evolution of a small-muscle polymorphism in lines of house mice selected for high activity levels. Evolution 56: 1267-1275.
25. Ge{ogonek}bczyński AK (2008) Nonshivering thermogenesis capacity versus basal metabolic rate in laboratory mice. J Therm Biol 33: 250-254.
26. Ge{ogonek}bczyński A, Konarzewski M (2009) Metabolic correlates of selection on aerobic capacity in laboratory mice: a test of the model for the evolution of endothermy. J Exp Biol 212: 2872-2878.
27. Ge{ogonek}bczyński A, Konarzewski M (2011) Effects of oxygen availability on maximum aerobic perfomance in Musmusculus selected for basal metabolic rate or aerobic capacity. J Exp Biol 214: 1714-1720.
28. Gienapp P, Teplitsky C, Alho JS, Mills JA, Merila J (2008) Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol 17: 167-178.
29. Girard I, Rezende EL, Garland T Jr (2007) Leptin levels and body composition of mice selectively bred for high voluntary activity. Physiol Biochem Zool 80: 568-579.
30. 2 delivery. J Appl Physiol 101: 1288-1296.
31. Goodacre R, Vaidyanathan S, Dunn WB, Harrigan GG, Kell DB (2004) Metabolomics by numbers: acquiring and understanding global metabolite data. Trends Biotechnol 22: 245-252.
32. Guderley H, Joanisse DR, Mokas S, Bilodeau GM, Garland T Jr (2008) Altered fiber types in gastrocnemius muscle of high wheel-running selected mice with mini muscle phenotypes. Comp Biochem Physiol B 149: 490-500.
33. Guertin DA, Kalyani VP, Bell GGW, Thoreen CC, Sabatini DM (2006) Functional genomics identifies TOR-regulated genes that control growth and division. Curr Biol 16: 958-970.
34. Haggerty C, Hoggard N, Brown DS, Clapham JC, Speakman JR (2008) Intra-specific variation in resting metabolic rate in MF1 mice is not associated with membrane lipid desaturation in the liver. Mech Ageing Dev 129: 129-137.
35. Hambly C, Adams A, Fustin JM, Rance KA, Bünger L, Speakman JR (2005) Mice with low metabolic rates are not susceptible to weight gain when fed a high-fat diet. Obes Res 13: 556-566.
36. Hartmann J, Garland T Jr, Hannon RM, Kelly SA, Muñoz G, Pomp D (2008) Fine mapping of "mini-muscle", a recessive mutation causing reduced hind-limb muscle mass in mice. J Hered 99: 679-687.
37. Hastings IM, Moruppa SM, Bunger L, Hill W (1997) Effect of selection on food intake in the adult mouse. J Anim Breed Genet 114: 419-433.
38. Hayes JP (2010) Metabolic rates, genetic constraints, and the evolution of endothermy. J Evol Biol 23: 1868-1877.
39. 2 uptake in rats selectively bred for endurance running capacity. J Appl Physiol 93: 1265-1274.
40. Howlett RA, Gonzalez NC, Wagner HE, Fu ZX, Britton SL, Koch LG, Wagner PD (2003) Genetic models in applied physiology-selected contribution: skeletal muscle capillarity and enzyme activity in rats selectively bred for running endurance. J Appl Physiol 94: 682-1688.
41. Hulbert AJ (2003) Life, death and membrane bilayers. J Exp Biol 206: 2303-2311.
42. Hulbert AJ, Else PL (1981) Comparison of the 'mammal machine and the 'reptile machine': energy use and thyroid activity. Am J Physiol 241: R350-R356.
43. Hulbert AJ, Else PL (1999) Membranes as possible pacemakers of metabolism. J Theor Biol 199: 257-274.
44. Hulbert AJ, Else PL (2000) Mechanisms underlying the cost of living in animals. Ann Rev Physiol 62: 207-235.
45. Hulbert AJ, Else PL (2005) Membranes and the setting of energy demand. J Exp Biol 208: 1593-1599.
46. Ives AR, Midford PE, Garland T Jr (2007) Within-species variation and measurement error in phylogenetic comparative methods. Sys Biol 56: 252-270.
47. Jacobson P, Rankinen T, Tremblay A, Pérusse L, Chagnon YC, Bouchard C (2006) Resting metabolic rate and respiratory quotient: results from a genome-wide scan in the Quebec Family Study. Am J Clin Nutr 84: 1527-1533.
48. Jasienski M, Bazzaz FA (1999) The fallacy of ratios and the testability of models in biology. Oikos 84: 321-326.
49. Javed F, He Q, Davidson LE, Thornton JC, Albu J, Boxt L, Krasnow N, Elia M, Kang P, Heshka S, Gallagher D (2010) Brain and high metabolic rate organ mass: contributions to resting energy expenditure beyond fat-free mass. Am J Clin Nutr 91: 907-912.
50. Johnson MS, Thomson SC, Speakman JR (2001a) Limits to sustained energy intake. I. Lactation in the laboratory mouse Mus musculus. J Exp Biol 204: 1925-1935.
51. Johnson MS, Thomson SC, Speakman JR (2001b) Limits to sustained energy intake II. Inter-relationships between resting metabolic rate, life-history traits and morphology in Mus musculus. J Exp Biol 204: 1446-1937.
52. Kaiyala KJ, Schwartz MW (2011) Toward a more complete (and less controversial) understanding of energy expenditure and its role in obesity pathogenesis. Diabetes 60: 17-23.
53. Kane SL, Garland T Jr, Carter PA (2008) Basal metabolic rate of aged mice is affected by random genetic drift but not by selective breeding for high early age locomotor activity or chronic wheel access. Physiol Biochem Zool 81: 288-300.
54. Kgwatalala PM, Nielsen MK (2004) Performance of mouse lines divergently selected for heat loss when exposed to different environmental temperatures. II. Feed intake, growth, fatness, and body organs. J Anim Sci 82: 2884-2891.
55. Kirkton SD, Howlett RA, Gonzales NC, Giuliano PG, Britton SL, Koch LG, Wagner HE, Wagner PD (2009) Continued artificial selection for running endurance in rats is associated with improved lung function. J Appl Physiol 106: 1810-1818.
56. Klaus S, Rudolph B, Dohrmann C, Wehr R (2005) Expression of uncoupling protein 1 in skeletal muscle decreases muscle energy efficiency and affects thermoregulation and substrate oxidation. Physiol Genomics 21: 193-200.
57. Koch LG, Britton SL (2001) Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol Genomics 5: 45-52.
58. Konarzewski M, Diamond J (1995) Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution 49: 1239-1248.
59. Konarzewski M, Ksia{ogonek}żek A, Łapo IB (2005) Artificial selection on metabolic rates and related traits in rodents. Integr Comp Biol 45: 416-425.
60. Koteja P (1996) Limits to the energy budget in a rodent, Peromyscus maniculatus: does gut capacity set the limit? Physiol Zool 69: 994-1020.
61. Koteja P (2000) Energy assimilation, parental care and the evolution of endothermy. Proc R Soc Lond B 267: 479-484.
62. Kozłowski J, Konarzewski M, Gawelczyk AT (2003) Cell size as a link between noncoding DNA and metabolic rate scaling. Proc Natl Acad Sci USA 24: 14080-14085.
63. Kozłowski J, Czarnołe{ogonek}ski M, Francois-Krassowska A, Maciak S, Pis T (2010) Cell size is positively correlated between different tissues in passerine birds and amphibians, but not necessarily in mammals. Biol Lett 6: 792-796.
64. Krogh A (1916) Respiratory exchange of animals and man. Longmans Green and Co, London.
65. Król EM, Johnson S, Speakman JR (2003) Limits to sustained energy intake VIII. Resting metabolic rate and organ morphology of laboratory mice lactating at thermoneutrality. J Exp Biol 206: 4283-4291.
66. Kruuk LEB (2004) Estimating genetic parameters in natural populations using the 'animal model'. Philos Trans R Soc B 359: 873-890.
67. Ksia{ogonek}żek A, Konarzewski M (2012) Effect of dietary restriction on immune response of laboratory mice divergently selected for basal metabolic rate. Physiol Biochem Zool 85: 51-61.
68. Ksia{ogonek}żek A, Konarzewski M, Chadzińska M, Cichoń M (2003) Costs of immune response in cold-stressed laboratory mice selected for high and low basal metabolism rates. Proc R Soc B 270: 2025-2031.
69. Ksia{ogonek}żek A, Konarzewski M, Łapo IB (2004) Anatomic and energetic correlates of divergent selection for basal metabolic rate in laboratory mice. Physiol Biochem Zool 77: 890-899.
70. Ksia{ogonek}żek A, Czerniecki J, Konarzewski M (2009) Phenotypic flexibility of traits related to energy acquisition in mice divergently selected for basal metabolic rate (BMR). J Exp Biol 212: 808-814.
71. Lacy RC, Lynch CB (1979) Quantitative genetic analysis of temperature regulation in Mus musculus I. Partitioning of variance. Genetics 91: 743-753.
72. Laplante M, Sabatini DM (2009) mTOR signaling at a glance. J Cell Sci 122: 3589-3594.
73. Later W, Bosy-Westphal A, Hitze B, Kossel E, Glüer CC, Heller M, Müller MJ (2008) No evidence of mass dependency of specific organ metabolic rate in healthy humans. Am J Clin Nutr 88: 1004-1009.
74. Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, Oxford.
75. Loos RJF, Rankinen T, Chagnon Y, Tremblay A, Pérusse L, Bouchard C (2006) Polymorphisms in the leptin and leptin receptor genes in relation to resting metabolic rate and respiratory quotient in the Québec Family Study. Int J Obes 30: 183-190.
76. Lynch CB, Sulzbach DS (1984) Quantitative genetic analysis of temperature regulation in Mus musculus. II. Diallel analysis of individual traits. Evolution 38: 527-540.
77. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland.
78. Maciak S, Janko K, Kotusz J, Choleva L, Boroń A, Juchno D, Kujawa R, Kozłowski J, Konarzewski M (2011) Standard metabolic rate (SMR) is inversely related to erythrocyte and genome size in allopolyploid fish of the Cobitis taenia hybrid complex. Funct Ecol 25: 1072-1078.
79. Malisch JL, Breuner CW, Kolb EM, Wada H, Hannon RM, Chappell MA, Middleton KM, Garland T Jr (2009) Behavioral despair and home-cage activity in mice with chronically elevated baseline corticosterone concentrations. Behav Genet 39: 192-201.
80. McDaneld TG, Nielsen MK, Miner LJ (2002) Uncoupling proteins and energy expenditure in mice divergently selected for heat loss. J Anim Sci 80: 602-608.
81. McNab BK (2002) The physiological ecology of vertebrates. Cornell University Press, Ithaca.
82. Middleton KM, Kelly SA, Garland T Jr (2008) Selective breeding as a tool to probe skeletal response to high voluntary locomotor activity in mice. Integr Comp Biol 48: 394-410.
83. Mitchell TW, Ekroos K, Blanksby SJ, Hulbert AJ, Else PE (2007) Differences in membrane acyl phospholipid composition between an endothermic mammal and an ectothermic reptile are not limited to any phospholipid class. J Exp Biol 210: 3440-3450.
84. Moody DE, Pomp D, Nielsen MK, van Vleck LD (1999) Identification of quantitative trait loci influencing traits related to energy balance in selection and inbred lines of mice. Genetics 152: 69-711.
85. Mousel MR, Stroup WW, Nielsen MK (2001) Locomotor activity, core body temperature, and circadian rhythms in mice selected for high or low heat loss. J Anim Sci 79: 861-868.
86. Müller MJ, Bosy-Westphal A, Kutzner D, Heller M (2002) Metabolically active components of fat-free mass and resting energy-expenditure in humans: recent lessons from imaging technologies. Obes Rev 3: 113-122.
87. Müller MJ, Langemann D, Gehrke I, Later W, Heller M, Glüer CC, Heymsfield SB, Bosy-Westphal A (2011) Effect of constitution on mass of individual organs and their association with metabolic rate in humans-a detailed view on allometric scaling. PLoS One 6: e22732.
88. Nachman MW, Hoekstra HE, D'Agostino SL (2003) The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad of Sci USA 100: 5268-5273.
89. Nespolo RF, Franco M (2007) Whole-animal metabolic rate is repeatable trait: a meta-analysis. J Exp Biol 210: 2000-2005.
90. Nespolo RF, Bacigalupe LD, Bozinovic F (2003) Heritability of energetics in a wild mammal, the leaf-eared mouse Phylottis darwini. Evolution 57: 1679-1688.
91. Nespolo RF, Bustamante DM, Bacigalupe LD, Bozinovic F (2005) Quantitative genetics of bioenergetics and growth-related traits in the wild mammal Phyllotis darwini. Evolution 59: 1829-1837.
92. Nespolo RF, Bacigalupe LD, Figueroa CC, Koteja P, Opazo JC (2011) Using new tools to solve an old problem: the evolution of endothermy in vertebrates. Trends Ecol Evol 26: 414-423.
93. Nielsen MK, Jones LD, Freking BA, DeShazer JA (1997a) Divergent selection for heat loss in mice. 1. Selection applied and direct response through fifteen generations. J Anim Sci 75: 1461-1468.
94. Nielsen MK, Freking BA, Jones LD, Nelson SM, Vorderstrasse TL, Hussey BA (1997b) Divergent selection for heatloss in mice. II. Correlated responses in feed intake, body mass, body composition, and number born through fifteen generations. J Anim Sci 75: 1469-1476.
95. Nilsson JÅ, Åkesson M, Nilsson JF (2009) Heritability of resting metabolic rate in a wild population of blue tits. J Evol Biol 22: 1867-1874.
96. Oleksiak MF, Churchill GA, Crawford DL (2002) Variation in gene expression within and among natural populations. Nat Genet 32: 261-266.
97. Packard GC, Boardman TJ (1987) The misuse of ratios to scale physiological data that vary allometrically with body size. In: Feder ME, Benett AF, Burggren WW, Huey RB (eds) New directions in ecological physiology. Cambridge University Press, Cambridge, pp 216-239.
98. Pemberton JM (2008) Wild pedigrees: the way forward. Proc R Soc B 275: 613-621.
99. Polymeropoulos ET, Heldmaier G, Frappell PB, McAllan BM, Withers KW, Klingenspor M, White CR, Jastroch M (2012) Phylogenetic differences of mammalian basal metabolic rate are not explained by mitochondrial basal proton leak. Proc R Soc B 279: 185-193.
100. Porter RK, Hulbert AJ, Brand MD (1996) Allometry of mitochondrial proton leak: influence of membrane surface area and fatty acid composition. Am J Physiol Reg I 271: R1550-R1560.
101. Raichlen DA, Gordon AD, Muchlinski MN, Snodgrass JJ (2010) Causes and significance of variation in mammalian basal metabolism. J Comp Physiol B 180: 301-311.
102. Ramanathan A, Schreiber SL (2009) Direct control of mitochondrial function by mTOR. Proc Natl Acad Sci USA 106: 22229-22232.
103. Rezende EL, Garland T Jr, Chappell MA, Malisch JL, Gomes FR (2006a) Maximum aerobic performance in lines of Mus selected for high wheel-running activity: effects of selection, oxygen availability, and the mini-muscle phenotype. J Exp Biol 209: 115-127.
104. Rezende EL, Kelly SA, Gomes FR, Chappell MA, Garland T Jr (2006b) Effects of size, sex and voluntary running speeds on costs of locomotion in lines of laboratory mice selectively bred for high wheel-running activity. Physiol Biochem Zool 79: 83-99.
105. Rezende EL, Gomes FR, Malisch JL, Chappell MA, Garland T Jr (2006c) Maximal oxygen consumption in relation to subordinate traits in lines of house mice selectively bred for high voluntary wheel running. J Appl Physiol 101: 477-485.
106. Rice T, Tremblay A, Dériaz O, Pérusse L, Rao DC, Bouchard C (1996) Genetic pleiotropy for resting metabolic rate with fat-free mass and fat mass: the Québec Family Study. Obes Res 4: 125-131.
107. Riska B, Prout T, Turelli M (1989) Laboratory estimates of heritabilities and genetic correlations in nature. Genetics 123: 865-871.
108. Roff DA (2002) Life history evolution. Sinauer, Sunderland.
109. Rokas A, Abbot P (2009) Harnessing genomics for evolutionary insights. Trends Ecol Evol 24: 192-200.
110. Rolfe DF, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77: 731-758.
111. Rolfe DF, Newman JM, Buckingham JA, Clark MG, Brand MD (1999) Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR. Am J Physiol 276: C692-C699.
112. Rønning B, Jensen H, Moe B, Bech C (2007) Basal metabolic rate: heritability and genetic correlations with morphological traits in the zebra finch. J Evol Biol 20: 1815-1822.
113. Sacher GA, Duffy PH (1979) Genetic relation of life span to metabolic rate for inbred strains and their hybrids. Fed Proc 38: 184-188.
114. Sadowska ET, Labocha MK, Baliga K, Stanisz A, Wróblewska AK, Jagusiak W, Koteja P (2005) Genetic correlations between basal and maximum metabolic rates in a wild rodent: consequences for evolution of endothermy. Evolution 59: 672-681.
115. Sadowska ET, Baliga-Klimczyk K, Chrza{ogonek}ścik KM, Koteja P (2008) Laboratory model of adaptive radiation: a selection experiment in the bank vole. Physiol Biochem Zool 81: 627-640.
116. Schieke SM, Phillips D, McCoy JP Jr, Aponte AM, Shen RF, Balaban RS, Finkel T (2006) The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J Biol Chem 281: 27643-27652.
117. Schmidt-Nielsen K (1984) Scaling: why is animal size so important?. Cambridge University Press, Cambridge.
118. Schmidt-Nielsen K (1997) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge.
119. Schwartz TS, Murray S, Seebacher F (2008) Novel reptilian uncoupling proteins: molecular evolution and gene expression during cold acclimation. Proc R Soc B 275: 979-985.
120. Seebacher F, Schwartz TS, Thompson MB (2006) Transition from ectothermy to endothermy: the development of metabolic capacity in a bird (Gallus gallus). Proc R Soc B 273: 565-570.
121. Selman CS, Lumsden L, Bunger L, Hill WG, Speakman JR (2001a) Resting metabolic rate and morphology in mice (Mus musculus) selected for high and low food intake. J Exp Biol 204: 777-784.
122. Selman C, Korhonen TK, Bunger L, Hill WG, Speakman JR (2001b) Thermoregulatory responses of two mouse Mus musculus strains selectively bred for high and low food intake. J Comp Physiol B 171: 661-668.
123. Shaw RG (1987) Maximum-likelihood approaches applied to quantitative genetics of natural populations. Evolution 41: 812-826.
124. Speakman JR, Talbot DA, Selman C, Snart S, McLaren JS, Redman P, Król E, Jackson DM, Johnson MS, Brand MD (2004) Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3: 87-95.
125. Stapley J, Reger J, Feulner PGD, Smadja C, Galindo J, Ekblom R, Bennison C, Ball AD, Beckerman AP, Slate J (2010) Adaptation genomics: the next generation. Trends Ecol Evol 25: 705-712.
126. Swallow JG, Carter PA, Garland T Jr (1998) Artificial selection for increased wheel running behavior in house mice. Behav Genet 28: 227-237.
127. Swallow JG, Rhodes JS, Garland T Jr (2005) Phenotypic and evolutionary plasticity of organ masses in response to voluntary exercise in house mice. Integr Comp Biol 45: 426-437.
128. Swallow JG, Hayes JB, Koteja P, Garland T Jr (2009) Selection experiments and experimental evolution of performance and physiology. In: Garland T Jr, Rose MR (eds) Experimental evolution: concepts, methods, and applications of selection experiments. University of California Press, Berkeley, pp 301-351.
129. Swallow JG, Wróblewska AK, Waters RP, Renner KJ, Britton SL, Koch LG (2010) Phenotypic and evolutionary plasticity of body composition in rats selectively bred for high endurance capacity. J Appl Physiol 109: 778-785.
130. Szafrańska PA, Zub K, Konarzewski M (2007) Long-term repeatability of body mass and resting metabolic rate in free-living weasels, Mustela nivalis. Funct Ecol 21: 731-737.
131. Thompson R (2008) Estimation of quantitative genetic parameters. Proc R Soc Lond B 275: 679-686.
132. Tracy CR, Sugar J (1989) Potential misuse of ANCOVA: comment on Packard and Boardman. Physiol Zool 62: 993-997.
133. Vaanholt LM, Meerlo P, Garland T Jr, Visser GH, van Dijk G (2007) Plasma adiponectin is increased in mice selectively bred for high wheel-running activity, but not by wheel running per sé. Horm Metab Res 39: 377-383.
134. Valencak TG, Ruf T (2007) N-3 polyunsaturated fatty acids impair lifespan but have no role for metabolism. Ageing Cell 6: 15-25.
135. Vera JC, Wheat CW, Fescemyer HW, Frilander MJ, Crawford DL, Hanski I, Marden JH (2008) Rapid transcriptome characterization for a nonmodel organism using 454 pyrosequencing. Mol Ecol 17: 1636-1647.
136. Wang Z, O'Conner TP, Heshka S, Heymsfield SB (2001) The reconstruction of Kleiber's law at the organ-tissue level. J Nutr 131: 2967-2970.
137. Wang Z, Ying Z, Bosy-Westphal A, Zhang J, Heller M, Later W, Heymsfield SB, Müller MJ (2011a) Evaluation of specific metabolic rates of major organs and tissues: comparison between men and women. Am J Hum Biol 23: 333-338.
138. Wang Z, Ying Z, Bosy-Westphal A, Zhang J, Heller M, Later W, Heymsfield SB, Müller MJ (2011b) Evaluation of specific metabolic rates of major organs and tissues: comparison between nonobese and obese women. Obesity doi: 10. 1038/oby. 2011. 256.
139. Wheat CW (2010) Rapidly developing functional genomics in ecological model systems via 454 transcriptome sequencing. Genetica 138: 433-451.
140. Wheat CW, Fescemeyer HW, Kvist ET, Vera C, Frilander M, Hanski I, Marden JH (2011) Functional genomics of life history variation in a butterfly metapopulation. Mol Ecol 20: 1813-1828.
141. White CR, Kearney MR (2012) Causes and consequences of variation in the basal metabolic rate of animals. J Comp Physiol B (in press).
142. Whitehead A (2012) Comparative genomics in ecological physiology: toward a more nuanced understanding of acclimation and adaptation. J Exp Biol 215: 884-891.
143. Whitehead A, Crawford DL (2006) Variation within and among species in gene expression: raw material for evolution. Mol Ecol 15: 1197-1211.
144. Wilson A, Rale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2009) An ecologist's guide to the animal model. J Anim Ecol 79: 13-26.
145. Wislöff U, Najjar SM, Ellingsen R, Haram PM, Swoap S, Al-Share Q, Fernström M, Rezaei K, Lee SJ, Koch LG, Britton SL (2005) Cardiovascular risk factors emerge after artificial selection for low aerobic capacity. Science 307: 418-420.
146. Wone B, Sears MW, Labocha MK, Donovan ER, Hayes JP (2009) Genetic variances and covariances of aerobic metabolic rates in laboratory mice. Proc R Soc B 276: 3695-3704.
147. Wone B, Donovan ER, Hayes JP (2011) Metabolomics of aerobic metabolism in mice selected for increased maximal metabolic rate. Comp Biochem Physiol D 6: 399-405.
148. Wu BJ, Else PL, Storlien LH, Hulbert AJ (2001) Molecular activity of Na+/K+-ATPase from different sources is related to the packing of membrane lipids. J Exp Biol 204: 4271-4280.
149. Wullschleger S, Loewith R, Hall MN (2006) TOR signaling in growth and metabolism. Cell 124: 471-484.
150. Zub K, Piertney S, Szafrańska P, Konarzewski M (2012) Environmental and genetic influences on body mass and resting metabolic rates (RMR) in the natural population of weasel Mustela nivalis. Mol Ecol 21(5): 1283-1293. doi: 10. 1111/j. 1365-294X. 2011. 05436. x.