Journal of Comparative Physiology B

, Volume 185, Issue 6, pp 587–606 | Cite as

Brown adipose tissue: physiological function and evolutionary significance

  • R. Oelkrug
  • E. T. Polymeropoulos
  • M. Jastroch


In modern eutherian (placental) mammals, brown adipose tissue (BAT) evolved as a specialized thermogenic organ that is responsible for adaptive non-shivering thermogenesis (NST). For NST, energy metabolism of BAT mitochondria is increased by activation of uncoupling protein 1 (UCP1), which dissipates the proton motive force as heat. Despite the presence of UCP1 orthologues prior to the divergence of teleost fish and mammalian lineages, UCP1’s significance for thermogenic adipose tissue emerged at later evolutionary stages. Recent studies on the presence of BAT in metatherians (marsupials) and eutherians of the afrotherian clade provide novel insights into the evolution of adaptive NST in mammals. In particular studies on the ‘protoendothermic’ lesser hedgehog tenrec (Afrotheria) suggest an evolutionary scenario linking BAT to the onset of eutherian endothermy. Here, we review the physiological function and distribution of BAT in an evolutionary context by focusing on the latest research on phylogenetically distinct species.


Brown adipose tissue Echinops telfairi Evolution Non-shivering thermogenesis Protoendotherm Uncoupling protein 1 



Brown adipose tissue


Non-shivering thermogenesis


Uncoupling protein 1



We would like to thank G. Heldmaier for editorial communication of this invited review. We also thank four critical anonymous reviewers for suggestions to improve the quality of this manuscript, and Silke Morin, Stacey Leigh Webb, Drs. Susanne Keipert and Carola Meyer for critical reading and editing.


  1. Adamsons K, Blumberg E, Joelsson I (1969) The effect of ambient temperature upon post-natal changes in oxygen consumption of the guinea-pig. J Physiol 202:261–269PubMedCentralPubMedGoogle Scholar
  2. Amiel JJ, Shine R (2012) Hotter nests produce smarter young lizards. Biol Lett 8:372–374. doi: 10.1098/rsbl.2011.1161 PubMedCentralPubMedGoogle Scholar
  3. Aquila H, Link TA, Klingenberg M (1985) The uncoupling protein from brown fat mitochondria is related to the mitochondrial ADP/ATP carrier. Analysis of sequence homologies and of folding of the protein in the membrane. EMBO J 4:2369–2376PubMedCentralPubMedGoogle Scholar
  4. Avery R (1979) Lizards: a study of thermoregulation. In: Institute of Biology’s Studies in Biology, vol 109Google Scholar
  5. Bakken G, Gates D (1975) Heat transfer analysis of animals: some implications for field ecology, physiology and evolution. In: Gates D, Schmerl R (eds) Perspectives in biophysical ecology. Springer, New York, pp 255–290Google Scholar
  6. Bakker RT (1971) Dinosaur physiology and the origin of mammals. Evolution 25:636–658. doi: 10.2307/2406945 Google Scholar
  7. Bal NC, Maurya SK, Sopariwala DH, Sahoo SK, Gupta SC, Shaikh SA (2012) Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals. Nat Med 18:1575–1579. doi: 10.1038/nm.2897 PubMedCentralPubMedGoogle Scholar
  8. Bartness TJ, Vaughan CH, Song CK (2010) Sympathetic and sensory innervation of brown adipose tissue. Int J Obes 34:36–42. doi: 10.1038/ijo.2010.182 Google Scholar
  9. Bell K, Blomberg S, Schwarzkopf L (2013) Detrimental influence on performance of high temperature incubation in a tropical reptile: is cooler better in the tropics? Oecologia 171:83–91. doi: 10.1007/s00442-012-2409-6 PubMedGoogle Scholar
  10. Bennett AF (1991) The evolution of activity capacity. J Exp Biol 160:1–23PubMedGoogle Scholar
  11. Bennett AF, Ruben JA (1979) Endothermy and activity in vertebrates. Science 206:649–654PubMedGoogle Scholar
  12. Berg F, Gustafson U, Andersson L (2006) The uncoupling protein 1 gene (UCP1) is disrupted in the pig lineage: a genetic explanation for poor thermoregulation in piglets. PLoS Genet 2:1178–1181. doi: 10.1371/journal.pgen.0020129 Google Scholar
  13. Bernson SM, Nicholls DG (1974) Acetate, a major end product of fatty-acid oxidation in hamster brown-adipose-tissue mitochondria. Eur J Biochem 47:517–525PubMedGoogle Scholar
  14. Berthon D, Herpin P, Le Dividic J (1995) Shivering is the main thermogenic mechanism in cold-exposed newborn pigs. Proc Nutr Soc 54:87Google Scholar
  15. Bicudo JE, Bianco AC, Vianna CR (2002) Adaptive thermogenesis in hummingbirds. J Exp Biol 205:2267–2273PubMedGoogle Scholar
  16. Block B (1991) Endothermy in fish: thermogenesis, ecology and evolution. In: Hochachka PW, Mommsen TP (eds) Biochemistry and molecular biology of fishes. Elsevier, New York, pp 269–311Google Scholar
  17. Böckler H, Steinlechner S, Heldmaier G (1982) Complete cold substitution of noradrenaline-induced thermogenesis in the Djungarian hamster, Phodopus sungorus. Experientia 38:261–262PubMedGoogle Scholar
  18. Boss O, Samec S, Kühne F, Bijlenga P, Assimacopoulos-Jeannet F, Seydoux J, Giacobino JP, Muzzin P (1998) Uncoupling protein-3 expression in rodent skeletal muscle is modulated by food intake but not by changes in environmental temperature. J Biol Chem 273:5–8PubMedGoogle Scholar
  19. Bouillaud F, Ricquier D, Thibault J, Weissenbach J (1985) Molecular approach to thermogenesis in brown adipose tissue: cDNA cloning of the mitochondrial uncoupling protein. Proc Natl Acad Sci USA 82:445–448PubMedCentralPubMedGoogle Scholar
  20. Brück K, Wünnenberg B (1966) Influence of ambient temperature in the process of replacement of nonshivering by shivering thermogenesis during postnatal development. Fed Proc 25:1332–1337PubMedGoogle Scholar
  21. Brück K, Wünnenberg W, Zeisberger E (1969) Comparison of cold-adaptive metabolic modifications in different species, with special reference to the miniature pig. Fed Proc 28:1035–1041PubMedGoogle Scholar
  22. Buffenstein R (1996) Ecophysiological responses to a subterranean habitat; a Bathyergid perspective. Mammalia 60:591–605Google Scholar
  23. Buffenstein R, Yahav S (1991) Is the naked mole rat Heterocephalus glaber an endothermic yet poikilothermic mammal? J Therm Biol 16:227–232Google Scholar
  24. Cambon B, Reyne Y, Nouguès J (1998) In vitro induction of UCP1 mRNA in preadipocytes from rabbit considered as a model of large mammals brown adipose tissue development: importance of PPARgamma agonists for cells isolated in the postnatal period. Mol Cell Endocrinol 146:49–58PubMedGoogle Scholar
  25. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277–359. doi: 10.1152/physrev.00015.2003 PubMedGoogle Scholar
  26. Cannon B, Vogel G (1977) The mitochondrial ATPase of brown adipose tissue. Purification and comparison with the mitochondrial ATPase from beef heart. FEBS Lett 76:284–289PubMedGoogle Scholar
  27. Cannon B, Romert L, Sundin U, Barnard T (1977) Morphology and biochemical properties of perirenal adipose tissue from lamb (Ovis aries). A comparison with brown adipose tissue. Comp Biochem Physiol B 56:87–99PubMedGoogle Scholar
  28. Carrière A, Jeanson Y, Berger-Müller S, André M, Chenouard V, Arnaud E, Barreau C, Walther R, Galinier A, Wdziekonski B, Villageois P, Louche K, Collas P, Moro C, Dani C, Villarroya F, Casteilla L (2014) Browning of white adipose cells by intermediate metabolites: an adaptive mechanism to alleviate redox pressure. Diabetes. doi: 10.2337/db13-1885 PubMedGoogle Scholar
  29. Carroll AM, Haines LR, Pearson TW, Fallon PG, Walsh CM, Brennan CM, Breen EP, Porter RK (2005) Identification of a functioning mitochondrial uncoupling protein 1 in thymus. J Biol Chem 280:15534–15543. doi: 10.1074/jbc.M413315200 PubMedGoogle Scholar
  30. Casteilla L, Champigny O, Bouillaud F, Robelin J, Ricquier D (1989) Sequential changes in the expression of mitochondrial protein mRNA during the development of brown adipose tissue in bovine and ovine species. Sudden occurrence of uncoupling protein mRNA during embryogenesis and its disappearance after birth. Biochem J 257:665–671PubMedCentralPubMedGoogle Scholar
  31. Chen JF, Zhong WQ, Wang DH (2012) Seasonal changes in body mass, energy intake and thermogenesis in Maximowiczi’s voles (Microtus maximowiczii) from the inner Mongolian grassland. J Comp Physiol B 182:275–285. doi: 10.1007/s00360-011-0608-9 PubMedGoogle Scholar
  32. Chi QS, Wang DH (2011) Thermal physiology and energetics in male desert hamsters (Phodopus roborovskii) during cold acclimation. J Comp Physiol B 181:91–103. doi: 10.1007/s00360-010-0506-6 PubMedGoogle Scholar
  33. Clarke KJ, Porter RK (2012) Uncoupling protein 1 dependent reactive oxygen species production by thymus mitochondria. Int J Biochem Cell Biol 45:81–89. doi: 10.1016/j.biocel.2012.09.023 PubMedGoogle Scholar
  34. Clarke DN, Zani PA (2012) Effects of night-time warming on temperate ectotherm reproduction: potential fitness benefits of climate change for side-blotched lizards. J Exp Biol 215:1117–11127. doi: 10.1242/jeb065359 PubMedGoogle Scholar
  35. Clarke L, Buss DS, Juniper DT, Lomax MA, Symonds ME (1997a) Adipose tissue development during early postnatal life in ewe-reared lambs. Exp Physiol 82:1015–1027PubMedGoogle Scholar
  36. Clarke L, Heasman L, Firth K, Symonds ME (1997b) Influence of route of delivery and ambient temperature on thermoregulation in newborn lambs. Am J Physiol 272:1931–1939Google Scholar
  37. Clements F, Hope P, Daniels C, Chapman I, Wittert G (1998) Thermogenesis in the marsupial Sminthopsis crassicaudata: effect of catecholamines and diet. Aust J Zool 46:381–390Google Scholar
  38. Coulter AA, Bearden CM, Liu X, Koza RA, Kozak LP (2003) Dietary fat interacts with QTLs controlling induction of Pgc-1α and Ucp1 during conversion of white to brown fat. Physiol Genomics 14:139–147PubMedGoogle Scholar
  39. Crompton AW, Taylor CR, Jagger JA (1978) Evolution of homeothermy in mammals. Nature 272:333–336PubMedGoogle Scholar
  40. Cypess AM, Lehman S, Williams G, Tal I, Rodman D, Goldfine AB, Kuo FC, Palmer EL, Tseng YH, Doria A, Kolodny GM, Kahn CR (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360:1509–1517. doi: 10.1056/NEJMoa0810780 PubMedCentralPubMedGoogle Scholar
  41. Cypess AM, White AP, Vernochet C, Schulz TJ, Xue R, Sass CA, Huang TL, Roberts-Toler C, Weiner LS, Sze C, Chacko AT, Deschamps LN, Herder LM, Truchan N, Glasgow AL, Holman AR, Gavrila A, Hasselgren PO, Mori MA, Molla M, Tseng YH (2013) Anatomical localization, gene expression profiling and functional characterization of adult human neck brown fat. Nat Med 19:635–669. doi: 10.1038/nm.3112 PubMedCentralPubMedGoogle Scholar
  42. Cypess AM, Haft CR, Laughlin MR, Hu HH (2014) Brown fat in humans: consensus points and experimental guidelines. Cell Metab 20:408–415. doi: 10.1016/j.cmet.2014.07.025 PubMedGoogle Scholar
  43. Darby CJ, Clarke L, Lomax MA, Symonds ME (1996) Brown adipose tissue and liver development during early postnatal life in hand-reared and ewe-reared lambs. Reprod Fertil Dev 8:137–145PubMedGoogle Scholar
  44. Dauncey MJ, Wooding FB, Ingram DL (1981) Evidence for the presence of brown adipose tissue in the pig. Res Vet Sci 31:76–81PubMedGoogle Scholar
  45. Dawson TJ, Olson JM (1988) Thermogenic capabilities of the opossum Monodelphis domestica when warm and cold acclimated: similarities between American and Australian marsupials. Comp Biochem Physiol A Comp Physiol 89:85–91PubMedGoogle Scholar
  46. Divakaruni AS, Brand MD (2011) The regulation and physiology of mitochondrial proton leak. Physiology 26:192–205. doi: 10.1152/physiol.00046.2010 PubMedGoogle Scholar
  47. Dlasková A, Clarke KJ, Porter RK (2010) The role of UCP 1 in production of reactive oxygen species by mitochondria isolated from brown adipose tissue. Biochim Biophys Acta 1797:1470–1476. doi: 10.1016/j.bbabio.2010.04.008 PubMedGoogle Scholar
  48. Downs CT, Perrin MR (1991) Physiological adjustments to low temperatures of four Gerbillurus species. J Therm Biol 16:25–29. doi: 10.1016/0306-4565(91)90047-6 Google Scholar
  49. Edson JL, Hull D, Elphick MC (1981) The development of cold-induced thermogenesis in hamsters. J Dev Physiol 3:387–396PubMedGoogle Scholar
  50. Else PL, Hulbert AJ (1981) Comparison of the “mammal machine” and the “reptile machine”: energy production. Am J Physiol 240:3–9Google Scholar
  51. Enerbäck S, Jacobsson A, Simpson EM, Guerra C, Yamashita H, Harper ME, Kozak LP (1997) Mice lacking mitochondrial uncoupling protein are cold-sensitive but not obese. Nature 387:90–94. doi: 10.1038/387090a0 PubMedGoogle Scholar
  52. Ewing LL, Schanbacher LM (1970) Early effects of experimental cryptorchidism on the activity of selected enzymes in rat testes. Endocrinology 87:129–134. doi: 10.1210/endo-87-1-129 PubMedGoogle Scholar
  53. Farmer C (2000) Parental care: the key to understanding endothermy and other convergent features in birds and mammals. Am Nat 155:326–334. doi: 10.1086/303323 PubMedGoogle Scholar
  54. Fedorenko A, Lishko PV, Kirichok Y (2012) Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell 151:400–413. doi: 10.1016/j.cell.2012.09.010 PubMedCentralPubMedGoogle Scholar
  55. Feist DD, Feist CF (1986) Effects of cold, short day and melatonin on thermogenesis, body weight and reproductive organs in Alaskan red-backed voles. J Comp Physiol B 156:741–746PubMedGoogle Scholar
  56. Feist DD, Rosenmann M (1975) Seasonal sympatho-adrenal and metabolic responses to cold in the Alaskan snowshoe hare (Lepus americanus macfarlani). Comp Biochem Physiol A Comp Physiol 51:449–455PubMedGoogle Scholar
  57. Fleury C, Neverova M, Collins S, Raimbault S, Champigny O, Levi-Meyrueis C, Bouillaud F, Seldin MF, Surwit RS, Ricquier D, Warden CH (1997) Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat Genet 15:269–272. doi: 10.1038/ng0397-269 PubMedGoogle Scholar
  58. Foster DO (1984) Quantitative contribution of brown adipose tissue thermogenesis to overall metabolism. Can J Biochem Cell Biol 62:618–622PubMedGoogle Scholar
  59. Geiser F (2008) Ontogeny and phylogeny of endothermy and torpor in mammals and birds. Comp Biochem Physiol A Mol Integr Physiol 150:176–180. doi: 10.1016/j.cbpa.2007.02.041 PubMedGoogle Scholar
  60. Gemmell RT, Bell AW, Alexander G (1972) Morphology of adipose cells in lambs at birth and during subsequent transition of brown to white adipose tissue in cold and in warm conditions. Am J Anat 133:143–163. doi: 10.1002/aja.1001330203 PubMedGoogle Scholar
  61. Génin F, Nibbelink M, Galand M, Perret M, Ambid L (2003) Brown fat and nonshivering thermogenesis in the gray mouse lemur (Microcebus murinus). Am J Physiol Regul Integr Comp Physiol 284:811–818. doi: 10.1152/ajpregu.00525.2002 Google Scholar
  62. Gesner C (1551) Conradi Gesneri medici Tigurini Historiae Animalium: Lib 1—De Quadrupedibus Viviparis (Zürich), 842Google Scholar
  63. Gettinger RD, Ralph CL (1985) Thermoregulatory responses to photoperiod by kangaroo rats (Dipodomys ordii): influence of night lighting on nonshivering thermogenesis and resting metabolism. J Exp Zool 234:335–340. doi: 10.1002/jez.1402340302 PubMedGoogle Scholar
  64. Gimeno RE, Dembski M, Weng X, Deng N, Shyjan AW, Gimeno CJ, Iris F, Ellis SJ, Woolf EA, Tartaglia LA (1997) Cloning and characterization of an uncoupling protein homolog: a potential molecular mediator of human thermogenesis. Diabetes 46:900–906PubMedGoogle Scholar
  65. Giralt M, Martin I, Iglesias R, Viñas O, Villarroya F, Mampel T (1990) Ontogeny and perinatal modulation of gene expression in rat brown adipose tissue. Unaltered iodothyronine 5′-deiodinase activity is necessary for the response to environmental temperature at birth. Eur J Biochem 193:297–302PubMedGoogle Scholar
  66. Golozoubova V, Hohtola E, Matthias A, Jacobsson A, Cannon B, Nedergaard J (2001) Only UCP1 can mediate adaptive nonshivering thermogenesis in the cold. FASEB J 15:2048–2050. doi: 10.1096/fj.00-0536fje PubMedGoogle Scholar
  67. Grigg GC, Beard LA, Augee ML (2004) The evolution of endothermy and its diversity in mammals and birds. Physiol Biochem Zool 77:982–997. doi: 10.1086/425188 PubMedGoogle Scholar
  68. Guerra C, Koza RA, Yamashita H, Wals K, Kozak LP (1998) Emergence of brown adipocytes in white fat in mice is under genetic control. Effects on body weight and adiposity. J Clin Invest 102:412–420PubMedCentralPubMedGoogle Scholar
  69. Gutowski JP, Wojciechowski MS, Jefimow M (2011) Diet affects resting, but not basal metabolic rate of normothermic Siberian hamsters acclimated to winter. Comp Biochem Physiol A Mol Integr Physiol 160:516–523. doi: 10.1016/j.cbpa.2011.08.012 PubMedGoogle Scholar
  70. Haim A (1981) Heat production and dissipation in a South african diurnal murid Lemniscomys griselda. South African J Zool 16:67–70Google Scholar
  71. Haim A (1984) Adaptive variations in heat production within Gerbils (genus Gerbillus) from different habitats. Oecologia 61:49–52. doi: 10.1007/BF00379087 Google Scholar
  72. Haim A (1987) Thermoregulation and metabolism of Wagner’s Gerbil (Gerbillus dasyurus): a rock dwelling rodent adapted to arid and mesic environments. J Therm Biol 12:45–48. doi: 10.1016/0306-4565(87)90022-2 Google Scholar
  73. Haim A (1996) Food and energy intake, non-shivering thermogenesis and daily rhythm of body temperature in the bushy-tailed gerbil Sekeetamys calurus: the role of photoperiod manipulations. J Therm Biol 21:37–42. doi: 10.1016/0306-4565(96)81275-7 Google Scholar
  74. Haim A, Fairall N (1986) Physiological adaptations to the subterranean environment by the mole rat Cryptomys hottentotus. Cimbebasia Ser 8A:49–53Google Scholar
  75. Haim A, Fairall N (1987) Bioenergetics of an herbivorous rodent Otomys irroratus. Physiol Zool 60:305–309. doi: 10.2307/30162283 Google Scholar
  76. Haim A, Fourie F (1980) Heat production in nocturnal (Praomys natalensis) and diurnal (Rhabdomys pumilio) South-African murids. South African J Zool 15:91–94Google Scholar
  77. Haim A, Harari J (1992) A comparative study of heat production and thermoregulation in two sympatric gerbils (Gerbillus gerbillus and G. pyramidum). Isr J Zool 38:363–372. doi: 10.1080/00212210.1992.10688683 Google Scholar
  78. Haim A, Izhaki I (1993) The ecological significance of resting metabolic rate and non-shivering thermogenesis for rodents. J Therm Biol 18:71–81. doi: 10.1016/0306-4565(93)90019-P Google Scholar
  79. Haim A, Levi G (1990) Role of body temperature in seasonal acclimatization: photoperiod-induced rhythms and heat production in Meriones crassus. J Exp Zool 256:237–241. doi: 10.1002/jez.1402560302 Google Scholar
  80. Haim A, Yahav S (1982) Non-shivering thermogenesis in winter-acclimatized and in long-scotophase and cold-acclimated Apodemus mystacinus (Rodentia). J Therm Biol 7:193–195. doi: 10.1016/0306-4565(82)90023-7 Google Scholar
  81. Haim A, Heth G, Avnon Z, Nevo E (1984) Adaptive physiological variation in nonshivering thermogenesis and its significance in speciation. J Comp Physiol B 154:145–147. doi: 10.1007/BF00684138 Google Scholar
  82. Haim A, Skinner JD, Robinson TJ (1987) Bioenergetics, thermoregulation and urine analysis of squirrels of the genus Xerus from an arid environment. South Afr J Zool 22:45–49Google Scholar
  83. Haim A, Racey PA, Speakman JR, Skinner JD (1991) Seasonal acclimatization and thermoregulation in the pouched mouse Saccostomus campestris. J Therm Biol 16:13–17. doi: 10.1016/0306-4565(91)90045-4 Google Scholar
  84. Haim A, McDevitt R, Speakman J (1995) Daily variations in the response of wood mice Apodemus sylvaticus to noradrenaline. J Exp Biol 198:561–565PubMedGoogle Scholar
  85. Haim A, Shabtay A, Arad Z (1998) Thermoregulatory responses of mesic and xeric rodent species to photoperiod manipulations. Comp Biochem Physiol A Mol Integr Physiol 120:187–191PubMedGoogle Scholar
  86. Hammel HT (1955) Thermal properties of fur. Am J Physiol 182:369–376PubMedGoogle Scholar
  87. Harms M, Seale P (2013) Brown and beige fat: development, function and therapeutic potential. Nat Med 19:1252–1263. doi: 10.1038/nm.3361 PubMedGoogle Scholar
  88. Hart JS (1952) Effects of temperature and work on metabolism, body temperature, and insulation: results with mice. Can J Zool 30:90–98. doi: 10.1139/z52-007 Google Scholar
  89. Hatai S (1902) On the presence in human embryos of an interscapular gland corresponding to the so-called hibernating gland of lower mammals. Ann Anat 21:369–373Google Scholar
  90. Hayes JP (1989) Altitudinal and seasonal effects on aerobic metabolism of deer mice. J Comp Physiol B 159:453–459PubMedGoogle Scholar
  91. Hayes JP, Garland T (1995) The evolution of endothermy: testing the aerobic capacity model. Evolution 49:836–847. doi: 10.2307/2410407 Google Scholar
  92. Hayward JS (1968) The magnitude of noradrenaline-induced thermogenesis in the bat (Myotis lucifugus) and its relation to arousal from hibernation. Can J Physiol Pharmacol 46:713–718PubMedGoogle Scholar
  93. Hayward JS, Lisson PA (1992) Evolution of brown fat: its absence in marsupials and monotremes. Can J Zool 70:171–179. doi: 10.1139/z92-025 Google Scholar
  94. Heath J (1968) Origins of thermoregulation. In: Drake E (ed) Evolution and environment. Yale University Press, New Haven, pp 259–278Google Scholar
  95. Heaton GM, Wagenvoord RJ, Kemp A, Nicholls DG (1978) Brown-adipose-tissue mitochondria: photoaffinity labelling of the regulatory site of energy dissipation. Eur J Biochem 82:515–521PubMedGoogle Scholar
  96. Heinrich B (1977) Why have some animals evolved to regulate a high body temperature? Am Nat 111:623–640. doi: 10.2307/2460321 Google Scholar
  97. Heldmaier G (1970) Die Thermogenese der Mausohrfledermaus (Myotis myotis) beim Erwachen aus dem Winterschlaf. Z vergl Physiol 63:59–84Google Scholar
  98. Heldmaier G (1971) Zitterfreie Wärmebildung und Körpergröße bei Säugetieren. Z vergl Physiol 73:222–248Google Scholar
  99. Heldmaier G, Steinlechner S, Rafael J, Vsiansky P (1981) Photoperiodic control and effects of melatonin on nonshivering thermogenesis and brown adipose tissue. Science 212:917–919PubMedGoogle Scholar
  100. Heldmaier G, Steinlechner S, Ruf T, Wiesinger H, Klingenspor M (1989) Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation. J Biol Rhythms 4:251–265PubMedGoogle Scholar
  101. Heldmaier G, Klaus S, Wiesinger H (1990) Seasonal adaptation of thermoregulatory heat production in small mammals. In: Voigt K, Bligh J (eds) Thermoreception and temperature regulation in mammals and birds. Springer, Berlin, pp 235–243Google Scholar
  102. Heldmaier G, Neuweiler G, Rössler W (2012) Vergleichende Tierphysiologie, 2nd edn. Springer Spektrum, BerlinGoogle Scholar
  103. Himms-Hagen J (1984) Thermogenesis in brown adipose tissue as an energy buffer. Implications for obesity. N Engl J Med 311:1549–1558. doi: 10.1056/NEJM198412133112407 PubMedGoogle Scholar
  104. Hislop MS, Buffenstein R (1994) Noradrenaline induces nonshivering thermogenesis in both the naked mole-rat (Heterocephalus glaber) and the Damara mole-rat (Cryptomys damarensis) despite very different modes of thermoregulation. J Therm Biol 19:25–32. doi: 10.1016/0306-4565(94)90006-X Google Scholar
  105. Hope PJ, Pyle D, Daniels CB, Chapman I, Horowitz M, Morley JE, Trayhurn P, Kumaratilake J, Wittert G (1997) Identification of brown fat and mechanisms for energy balance in the marsupial, Sminthopsis crassicaudata. Am J Physiol 273:161–167Google Scholar
  106. Houstĕk J, Janíková D, Bednár J, Kopecký J, Sebestián J, Soukup T (1990) Postnatal appearance of uncoupling protein and formation of thermogenic mitochondria in hamster brown adipose tissue. Biochim Biophys Acta 1015:441–449PubMedGoogle Scholar
  107. Hsieh A, Carlson L (1957) Role of adrenaline and noradrenaline in chemical regulation of heat production. Am J Physiol 190:243–246PubMedGoogle Scholar
  108. Hughes DA, Jastroch M, Stoneking M, Klingenspor M (2009) Molecular evolution of UCP1 and the evolutionary history of mammalian non-shivering thermogenesis. BMC Evol Biol 9:4. doi: 10.1186/1471-2148-9-4 PubMedCentralPubMedGoogle Scholar
  109. Hulbert AJ (1980) The evolution of energy metabolism in mammals. In: Schmidt-Nielsen K, Bolis L, Taylor C (eds) Comparative physiology: primitive mammals. Cambridge University Press, Cambridge, pp 129–139Google Scholar
  110. IUPS-Thermal-Commission (2003) Glossary of terms for thermal physiology. J Therm Biol 28:75–106. doi: 10.1016/S0306-4565(02)00055-4 Google Scholar
  111. Jamieson L, Stribling D, Rothwell NJ, Stock MJ (1984) Effect of noradrenaline on oxygen consumption and tissue blood flow in young pigs. Can J Physiol Pharmacol 62:136–141PubMedGoogle Scholar
  112. Janský L (1969) Comparative aspects of cold acclimation and nonshivering thermogenesis in homeotherms. Int J Biometeorol 13:199–209PubMedGoogle Scholar
  113. Janský L (1973) Non-shivering thermogenesis and its thermoregulatory significance. Biol Rev Camb Philos Soc 48:85–132PubMedGoogle Scholar
  114. Janský L, Hart JS (1963) Participation of skeletal muscle and kidney during nonshivering thermogenesis in cold-acclimated rats. Can J Biochem Physiol 41:953–964. doi: 10.1139/o63-108 PubMedGoogle Scholar
  115. Jastroch M, Withers K, Klingenspor M (2004) Uncoupling protein 2 and 3 in marsupials: identification, phylogeny, and gene expression in response to cold and fasting in Antechinus flavipes. Physiol Genomics 17:130–139. doi: 10.1152/physiolgenomics.00165.2003 PubMedGoogle Scholar
  116. Jastroch M, Wuertz S, Kloas W, Klingenspor M (2005) Uncoupling protein 1 in fish uncovers an ancient evolutionary history of mammalian nonshivering thermogenesis. Physiol Genomics 22:150–156. doi: 10.1152/physiolgenomics.00070.2005 PubMedGoogle Scholar
  117. Jastroch M, Buckingham JA, Helwig M, Klingenspor M, Brand MD (2007) Functional characterization of UCP1 in the common carp: uncoupling activity in liver mitochondria and cold-induced expression in the brain. J Comp Physiol B 177:743–752. doi: 10.1007/s00360-007-0171-6 PubMedGoogle Scholar
  118. Jastroch M, Withers KW, Taudien S, Frappell PB, Helwig M, Fromme T, Hirschberg V, Heldmaier G, McAllan BM, Firth BT, Burmester T, Platzer M, Klingenspor M (2008) Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis. Physiol Genomics 32:161–169. doi: 10.1152/physiolgenomics.00183.2007 PubMedGoogle Scholar
  119. Jastroch M, Divakaruni AS, Mookerjee S, Treberg JR, Brand MD (2010) Mitochondrial proton and electron leaks. Essays Biochem 47:53–67. doi: 10.1042/bse0470053 PubMedCentralPubMedGoogle Scholar
  120. Jastroch M, Hirschberg V, Klingenspor M (2012) Functional characterization of UCP1 in mammalian HEK293 cells excludes mitochondrial uncoupling artefacts and reveals no contribution to basal proton leak. Biochim Biophys Acta 1817:1660–1670. doi: 10.1016/j.bbabio.2012.05.014 PubMedGoogle Scholar
  121. Joly J, Saint-Girons H (1975) Influence de la température sur la vitesse de la esperematogènese, la durée de l’activité spermatogénétique et l’évolution des caractères secondaires du lézard des murailles, Lacerta muralis L. (Reptilia, Lacertidae). Arch Anat Microsc Morph Exp 64:317–336Google Scholar
  122. Kaciuba-Uściłko H, Poczopko P (1973) The effect of noradrenaline on heat production in the new-born pig. Experientia 29:108–109. doi: 10.1007/BF01913283 PubMedGoogle Scholar
  123. Keipert S, Jastroch M (2014) Brite/beige fat and UCP1—is it thermogenesis? Biochim Biophys Acta 1837:1075–1082. doi: 10.1016/j.bbabio.2014.02.008 PubMedGoogle Scholar
  124. Keipert S, Klaus S, Heldmaier G, Jastroch M (2010) UCP1 ectopically expressed in murine muscle displays native function and mitigates mitochondrial superoxide production. Biochim Biophys Acta 1797:324–330. doi: 10.1016/j.bbabio.2009.11.008 PubMedGoogle Scholar
  125. Kim EB, Fang X, Fushan AA, Huang Z, Lobanov AV, Han L, Marino SM, Sun X, Turanov AA, Yang P, Yim SH, Zhao X, Kasaikina MV, Stoletzki N, Peng C, Polak P, Xiong Z, Kiezun A, Zhu Y, Chen Y, Kryukov GV, Zhang Q, Peshkin L, Yang L et al (2011) Genome sequencing reveals insights into physiology and longevity of the naked mole rat. Nature 479:223–227. doi: 10.1038/nature10533 PubMedCentralPubMedGoogle Scholar
  126. Klaus S, Heldmaier G, Ricquier D (1988) Seasonal acclimation of bank voles and wood mice: nonshivering thermogenesis and thermogenic properties of brown adipose tissue mitochondria. J Comp Physiol B 158:157–164PubMedGoogle Scholar
  127. Klingenberg M, Huang SG (1999) Structure and function of the uncoupling protein from brown adipose tissue. Biochim Biophys Acta 1415:271–296PubMedGoogle Scholar
  128. Klingenberg M, Winkler E (1985) The reconstituted isolated uncoupling protein is a membrane potential driven H+ translocator. EMBO J 4:3087–3092PubMedCentralPubMedGoogle Scholar
  129. Koteja P (2000) Energy assimilation, parental care and the evolution of endothermy. Proc Biol Sci 267:479–484. doi: 10.1098/rspb.2000.1025 PubMedCentralPubMedGoogle Scholar
  130. Koza RA, Hohmann SM, Guerra C, Rossmeisl M, Kozak, LP (2000) Synergistic gene interactions control the induction of the mitochondrial uncoupling protein (Ucp1) gene in white fat tissue. J Biol Chem 275:34486–34492. doi: 10.1074/jbc.M002136200
  131. Kozłowski J (1992) Optimal allocation of resources to growth and reproduction: implications for age and size at maturity. Trends Ecol Evol 7:15–19. doi: 10.1016/0169-5347(92)90192-E PubMedGoogle Scholar
  132. Kozłowski J, Weiner J (1997) Interspecific allometries are by-products of body size optimization. Am Nat 149:352–380. doi: 10.2307/2463399 Google Scholar
  133. Król E, Martin SAM, Huhtaniemi IT, Douglas A, Speakman JR (2011) Negative correlation between milk production and brown adipose tissue gene expression in lactating mice. J Exp Biol 214:4160–4170. doi: 10.1242/jeb.061382 PubMedGoogle Scholar
  134. Kronfeld-Schor N, Haim A, Dayan T, Zisapel N, Klingenspor M, Heldmaier G (2000) Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice. Physiol Biochem Zool 73:37–44. doi: 10.1086/316718 PubMedGoogle Scholar
  135. Laloi M, Klein M, Riesmeier JW, Müller-Röber B, Fleury C, Bouillaud F, Ricquier D (1997) A plant cold-induced uncoupling protein. Nature 389:135–136. doi: 10.1038/38156 PubMedGoogle Scholar
  136. Lavocat R (1978) Rodentia and lagomorpha. In: Magio V, Cooke H (eds) Evolution of African mammals. Havard University Press, Cambridge, pp 68–89Google Scholar
  137. Lean MEJ (1989) Brown adipose tissue in humans. Proc Nutr Soc 48:243–256PubMedGoogle Scholar
  138. Lee Y-H, Petkova AP, Mottillo EP, Granneman JG (2012) In vivo identification of bipotential adipocyte progenitors recruited by β3-adrenoceptor activation and high fat feeding. Cell Metab 15:480–491. doi: 10.1016/j.cmet.2012.03.009 PubMedCentralPubMedGoogle Scholar
  139. Levesque DL, Lovegrove BG (2014) Increased homeothermy during reproduction in a basal placental mammal. J Exp Biol 217:1535–1542. doi: 10.1242/jeb.098848 PubMedGoogle Scholar
  140. Levesque D, Lobban K, Lovegrove B (2014) Effects of reproductive status and high ambient temperatures on the body temperature of a free-ranging basoendotherm. J Comp Physiol B. doi: 10.1007/s00360-014-0858-4 PubMedGoogle Scholar
  141. Li XS, Wang DH (2005) Seasonal adjustments in body mass and thermogenesis in Mongolian gerbils (Meriones unguiculatus): the roles of short photoperiod and cold. J Comp Physiol B 175:593–600. doi: 10.1007/s00360-005-0022-2 PubMedGoogle Scholar
  142. Li Q, Sun R, Huang C, Wang Z, Liu X, Hou J, Liu J, Cai L, Li N, Zhang S, Wang Y (2001) Cold adaptive thermogenesis in small mammals from different geographical zones of China. Comp Biochem Physiol A Mol Integr Physiol 129:949–961PubMedGoogle Scholar
  143. Licht P (1972) Actions of mammalian pituitary gonadotropins (FSH and LH) in reptiles. Gen Comp Endocrinol 19:282–289. doi: 10.1016/0016-6480(72)90108-6 PubMedGoogle Scholar
  144. Lidell ME, Betz MJ, Dahlqvist Leinhard O, Heglind M, Elander L, Slawik M, Mussack T, Nilsson D, Romu T, Nuutila P, Virtanen KA, Beuschlein F, Persson A, Borga M, Enerbäck S (2013) Evidence for two types of brown adipose tissue in humans. Nat Med 19:631–634. doi: 10.1038/nm.3017 PubMedGoogle Scholar
  145. Lin CS, Klingenberg M (1982) Characteristics of the isolated purine nucleotide binding protein from brown fat mitochondria. Biochemistry 21:2950–2956. doi: 10.1021/bi00541a023 PubMedGoogle Scholar
  146. Loncar D, Afzelius BA, Cannon B (1988) Epididymal white adipose tissue after cold stress in rats. I. Nonmitochondrial changes. J Ultrastruct Mol Struct Res 101:109–122PubMedGoogle Scholar
  147. Loudon A, Rothwell N, Stock M (1985) Brown fat, thermogenesis and physiological birth in a marsupial. Comp Biochem Physiol Part A Physiol 81:815–819. doi: 10.1016/0300-9629(85)90912-0 Google Scholar
  148. Lovegrove BG (2012a) The evolution of mammalian body temperature: the Cenozoic supraendothermic pulses. J Comp Physiol B 182:579–589. doi: 10.1007/s00360-011-0642-7 PubMedGoogle Scholar
  149. Lovegrove BG (2012b) The evolution of endothermy in Cenozoic mammals: a plesiomorphic-apomorphic continuum. Biol Rev Camb Philos Soc 87:128–162. doi: 10.1111/j.1469-185X.2011.00188.x PubMedGoogle Scholar
  150. Lovegrove BG, Génin F (2008) Torpor and hibernation in a basal placental mammal, the lesser hedgehog tenrec Echinops telfairi. J Comp Physiol B 178:691–698. doi: 10.1007/s00360-008-0257-9 PubMedGoogle Scholar
  151. Lovegrove BG, Heldmaier G, Knight M (1991) Seasonal and circadian energetic patterns in an arboreal rodent, Thallomys paedulcus, and a burrow-dwelling rodent, Aethomys namaquensis, from the Kalahari Desert. J Therm Biol 16:199–209. doi: 10.1016/0306-4565(91)90026-X Google Scholar
  152. Lowell BB, Spiegelman BM (2000) Towards a molecular understanding of adaptive thermogenesis. Nature 404:652–660. doi: 10.1038/35007527 PubMedGoogle Scholar
  153. Luna F, Roca P, Oliver J, Antenucci CD (2012) Maximal thermogenic capacity and non-shivering thermogenesis in the South American subterranean rodent Ctenomys talarum. J Comp Physiol B 182:971–983. doi: 10.1007/s00360-012-0675-6 PubMedGoogle Scholar
  154. Lynch GR, White S, Grundel R, Berger M (1978) Effects of photoperiod, melatonin administration and thyroid block on spontaneous daily torpor and temperature regulation in the white-footed mouse, Peromyscus leucopus. J Comp Physiol 125:157–163. doi: 10.1007/BF00686752 Google Scholar
  155. Maier HA, Feist DD (1991) Thermoregulation, growth, and reproduction in Alaskan collared lemmings: role of short day and cold. Am J Physiol 261:522–530Google Scholar
  156. McDevitt RM, Speakman JR (1996) Summer acclimatization in the short-tailed field vole, Microtus agrestis. J Comp Physiol B 166:286–293PubMedGoogle Scholar
  157. McNab BK (1978) The evolution of endothermy in the phylogeny of mammals. Am Nat 112:1–21. doi: 10.2307/2460134 Google Scholar
  158. Merritt JF (1995) Seasonal thermogenesis and changes in body mass of Masked shrews, Sorex cinereus. J Mammal 76:1020–1035. doi: 10.2307/1382596 Google Scholar
  159. Merritt JF, Zegers DA (1991) Seasonal thermogenesis and body-mass dynamics of Clethrionomys gapperi. Can J Zool 69:2771–2777. doi: 10.1139/z91-390 Google Scholar
  160. Merritt JF, Zegers DA, Rose LR (2001) Seasonal thermogenesis of Southern flying squirrels (Glaucomys volans). J Mammal 82:51–64. doi: 10.2307/1383679 Google Scholar
  161. Mills EM, Banks ML, Sprague JE, Finkel T (2003) Pharmacology: uncoupling the agony from ecstasy. Nature 426:403–404PubMedGoogle Scholar
  162. Miroux B, Frossard V, Raimbault S, Ricquier D, Bouillaud F (1993) The topology of the brown adipose tissue mitochondrial uncoupling protein determined with antibodies against its antigenic sites revealed by a library of fusion proteins. EMBO J 12:3739–3745PubMedCentralPubMedGoogle Scholar
  163. Morrison SF, Madden CJ, Tupone D (2014) Central neural regulation of brown adipose tissue thermogenesis and energy expenditure. Cell Metab 19:741–756. doi: 10.1016/j.cmet.2014.02.007 PubMedCentralPubMedGoogle Scholar
  164. Moshkin MP, Novikov EA, Petrovski DV (2011) Seasonal changes of thermoregulation in the mole vole Ellobius talpinus. Physiol Biochem Zool 74:869–875. doi: 10.1086/324750 Google Scholar
  165. Mount (1968) The climatic physiology of the pig. The Camelot Press, London and Southampton, p 76Google Scholar
  166. Mouroux I, Bertin R, Portet R (1990) Thermogenic capacity of the brown adipose tissue of developing rats; effects of rearing temperature. J Dev Physiol 14:337–342PubMedGoogle Scholar
  167. Murphy WJ, Eizirik E, O’Brien SJ, Madsen O, Scally M, Douady CJ, Teeling E, Ryder OA, Stanhope MJ, de Jong WW, Springer MS (2001) Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351. doi: 10.1126/science.1067179 PubMedGoogle Scholar
  168. Mzilikazi N, Lovegrove BG (2006) Noradrenalin induces thermogenesis in a phylogenetically ancient eutherian mammal, the rock elephant shrew, Elephantulus myurus. J Comp Physiol B 176:75–84. doi: 10.1007/s00360-005-0035-x PubMedGoogle Scholar
  169. Mzilikazi N, Lovegrove BG, Ribble DO (2002) Exogenous passive heating during torpor arousal in free-ranging rock elephant shrews, Elephantulus myurus. Oecologia 133:307–314. doi: 10.2307/4223422 Google Scholar
  170. Mzilikazi N, Jastroch M, Meyer CW, Klingenspor M (2007) The molecular and biochemical basis of nonshivering thermogenesis in an African endemic mammal, Elephantulus myurus. Am J Physiol Regul Integr Comp Physiol 293:2120–2127. doi: 10.1152/ajpregu.00427.2007 Google Scholar
  171. Nagasaka T, Carlson L (1965) Responses of cold- and warm-adapted dogs to infused norepinephrine and acute body cooling. Am J Physiol 209:227–230PubMedGoogle Scholar
  172. Nakamura K, Morrison SF (2008) A thermosensory pathway that controls body temperature. Nat Neurosci 11:62–71. doi: 10.1038/nn2027 PubMedCentralPubMedGoogle Scholar
  173. Nautiyal KM, Dailey M, Brito N, Brito MNDA, Harris RB, Bartness TJ, Grill HJ (2008) Energetic responses to cold temperatures in rats lacking forebrain-caudal brain stem connections. Am J Physiol Regul Integr Comp Physiol 295:789–798. doi: 10.1152/ajpregu.90394.2008 Google Scholar
  174. Nedergaard J, Cannon B (2003) The “novel” “uncoupling” proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions. Exp Physiol 88:65–84PubMedGoogle Scholar
  175. Nedergaard J, Cannon B (2013a) How brown is brown fat? It depends where you look. Nat Med 19:540–541. doi: 10.1038/nm.3187 PubMedGoogle Scholar
  176. Nedergaard J, Cannon B (2013b) UCP1 mRNA does not produce heat. Biochim Biophys Acta 1831:943–949. doi: 10.1016/j.bbalip.2013.01.009 PubMedGoogle Scholar
  177. Nedergaard J, Cannon B (2014) The browning of white adipose tissue: some burning issues. Cell Metab 20:396–407. doi: 10.1016/j.cmet.2014.07.005 PubMedGoogle Scholar
  178. Nedergaard J, Connolly E, Cannon B (1986) Brown adipose tissue in the mammalian neonate. In: Trayhurn P, Nicholls D (eds) Brown adipose tissue. Arnold, London, pp 152–213Google Scholar
  179. Nedergaard J, Bengtsson T, Cannon B (2007) Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 293:444–452. doi: 10.1152/ajpendo.00691.2006 Google Scholar
  180. Nespolo R, Opazo J, Rosenmann M, Bozinovic F (1999) Thermal acclimation, maximum metabolic rate and non-shivering thermogenesis of Phylottis xanthopygus (Rodentia) in the Andes mountains. J Mammal 80:742–748Google Scholar
  181. Nespolo RF, Bacigalupe LD, Rezende EL, Bozinovic F (2001) When nonshivering thermogenesis equals maximum metabolic rate: thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyanus (Rodentia). Physiol Biochem Zool 74:325–332. doi: 10.1086/320420 PubMedGoogle Scholar
  182. Nibbelink M, Moulin K, Arnaud E, Duval C, Pénicaud L, Casteilla L (2001) Brown fat UCP1 is specifically expressed in uterine longitudinal smooth muscle cells. J Biol Chem 276:47291–47295PubMedGoogle Scholar
  183. Nicholls DG, Locke RM (1984) Thermogenic mechanisms in brown fat. Physiol Rev 64:1–64PubMedGoogle Scholar
  184. Nicol SC (1978) Non-shivering thermogenesis in the potoroo, Potorous tridactylus (Kerr). Comp Biochem Physiol Part C Comp Pharmacol 59:33–37. doi: 10.1016/0306-4492(78)90008-4 Google Scholar
  185. Nicol SC, Pavlides D, Andersen NA (1997) Nonshivering thermogenesis in marsupials: absence of thermogenic response to beta 3-adrenergic agonists. Comp Biochem Physiol A Physiol 117:399–405PubMedGoogle Scholar
  186. Nicol SC, Andersen NA, Arnold W, Ruf T (2009) Rewarming rates of two large hibernators: comparison of a monotreme and a eutherian. J Therm Biol 34:155–159. doi: 10.1016/j.jtherbio.2009.01.003 Google Scholar
  187. Nowack J, Dausmann KH, Mzilikazi N (2013) Nonshivering thermogenesis in the African lesser bushbaby, Galago moholi. J Exp Biol 216:3811–3817. doi: 10.1242/jeb.089433 PubMedGoogle Scholar
  188. Oelkrug R, Kutschke M, Meyer CW, Heldmaier G, Jastroch M (2010) Uncoupling protein 1 decreases superoxide production in brown adipose tissue mitochondria. J Biol Chem 285:21961–21968PubMedCentralPubMedGoogle Scholar
  189. Oelkrug R, Heldmaier G, Meyer CW (2011) Torpor patterns, arousal rates, and temporal organization of torpor entry in wildtype and UCP1-ablated mice. J Comp Physiol B 181:137–145. doi: 10.1007/s00360-010-0503-9 PubMedGoogle Scholar
  190. Oelkrug R, Meyer CW, Heldmaier G, Mzilikazi N (2012) Seasonal changes in thermogenesis of a free-ranging afrotherian small mammal, the Western rock elephant shrew (Elephantulus rupestris). J Comp Physiol B 182:715–727. doi: 10.1007/s00360-012-0647-x PubMedGoogle Scholar
  191. Oelkrug R, Goetze N, Exner C, Lee Y, Ganjam GK, Kutschke M, Müller S, Stöhr S, Tschöp MH, Crichton PG, Heldmaier G, Jastroch M, Meyer CW (2013) Brown fat in a protoendothermic mammal fuels eutherian evolution. Nat Commun 4:2140PubMedCentralPubMedGoogle Scholar
  192. Oelkrug R, Goetze N, Meyer CW, Jastroch M (2014) Antioxidant properties of UCP1 are evolutionarily conserved in mammals and buffer mitochondrial reactive oxygen species. Free Radic Biol Med 77:210–216. doi: 10.1016/j.freeradbiomed.2014.09.004 PubMedGoogle Scholar
  193. Opazo JC, Nespolo RF, Bozinovic F (1999) Arousal from torpor in the Chilean mouse-opposum (Thylamys elegans): does non-shivering thermogenesis play a role? Comp Biochem Physiol A Mol Integr Physiol 123:393–397PubMedGoogle Scholar
  194. Polymeropoulos ET, Jastroch M, Frappell PB (2012) Absence of adaptive nonshivering thermogenesis in a marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata). J Comp Physiol B 182:393–401. doi: 10.1007/s00360-011-0623-x PubMedGoogle Scholar
  195. Pope M, Budge H, Symonds ME (2014) The developmental transition of ovine adipose tissue through early life. Acta Physiol 210:20–30. doi: 10.1111/apha.12053 Google Scholar
  196. Poppitt SD, Speakman JR, Racey PA (1994) Energetics of reproduction in the lesser hedgehog tenrec, Echinops telfairi (Martin). Physiol Zool 67:976–994. doi: 10.2307/30163874 Google Scholar
  197. Raimbault S, Dridi S, Denjean F, Lachuer J, Couplan E, Bouillaud F, Bordas A, Duchamp C, Taouis M, Ricquier D (2001) An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds. Biochem J 353:441–444PubMedCentralPubMedGoogle Scholar
  198. Rasmussen AT (1923) The so-called hibernating gland. J Morphol 38:147–205. doi: 10.1002/jmor.1050380106 Google Scholar
  199. Richter TA, Webb PI, Skinner JD (1997) Limits to the distribution of the southern African ice rat (Otomys sloggetti): thermal physiology or competitive exclusion? Funct Ecol 11:240–246. doi: 10.1046/j.1365-2435.1997.00078.x Google Scholar
  200. Rodriguez-Serrano E, Bozinovic F (2009) Interplay between global patterns of environmental temperature and variation in nonshivering thermogenesis of rodent species across large spatial scales. Glob Chang Biol 15:2116–2122. doi: 10.1111/j.1365-2486.2009.01854.x Google Scholar
  201. Rose RW, Kuswanti N, Colquhoun EQ (1998) Development of endothermy in a Tasmanian marsupial, Bettongia gaimardi and its response to cold and noradrenaline. J Comp Physiol B 168:359–363PubMedGoogle Scholar
  202. Rose RW, West AK, Ye JM, McCormick GH, Colquhoun EQ (1999) Nonshivering thermogenesis in a marsupial (the tasmanian bettong Bettongia gaimardi) is not attributable to brown adipose tissue. Physiol Biochem Zool 72:699–704. doi: 10.1086/316709 PubMedGoogle Scholar
  203. Rosenwald M, Perdikari A, Rülicke T, Wolfrum C (2013) Bi-directional interconversion of brite and white adipocytes. Nat Cell Biol 15:659–667PubMedGoogle Scholar
  204. Rothwell NJ, Stock MJ (1985a) Biological distribution and significance of brown adipose tissue. Comp Biochem Physiol A Comp Physiol 82:745–751PubMedGoogle Scholar
  205. Rothwell NJ, Stock MJ (1985b) Thermogenic capacity and brown adipose tissue activity in the common marmoset. Comp Biochem Physiol A Comp Physiol 81:683–686PubMedGoogle Scholar
  206. Rousset S, Alves-Guerra MC, Ouadghiri-Bencherif S, Kozak LP, Miroux B, Richard D, Bouillaud F, Ricquier D, Cassard-Doulcier AM (2003) Uncoupling Protein 2, but not uncoupling protein 1, is expressed in the female mouse reproductive tract. J Biol Chem 278:45843–45847PubMedGoogle Scholar
  207. Rousset S, Alves-Guerra M-C, Mozo J, Miroux B, Cassard-Doulcier A-M, Bouillaud F, Ricquier D (2004) The biology of mitochondrial uncoupling proteins. Diabetes 53:130–135Google Scholar
  208. Rowlatt U, Mrosovsky N, English A (1971) A comparative survey of brown fat in the neck and axilla of mammals at birth. Biol Neonate 17:53–83PubMedGoogle Scholar
  209. Ruben J (1995) The evolution of endothermy in mammals and birds: from physiology to fossils. Annu Rev Physiol 57:69–95. doi: 10.1146/ PubMedGoogle Scholar
  210. Saarela S, Hissa R (1993) Metabolism, thermogenesis and daily rhythm of body temperature in the wood lemming, Myopus schisticolor. J Comp Physiol B 163:546–555PubMedGoogle Scholar
  211. Scantlebury M, Afik D, Shanas U, Haim A (2002) Comparative non-shivering thermogenesis in adjacent populations of the common spiny mouse (Acomys cahirinus) from opposite slopes: the effects of increasing salinity. J Comp Physiol B 172:1–5PubMedGoogle Scholar
  212. Scantlebury M, Shanas U, Kupshtein H, Afik D, Haim A (2003) Non-shivering thermogenesis in common spiny mice Acomys cahirinus from adjacent habitats: response to seasonal acclimatization and salinity acclimation. J Therm Biol 28:287–293. doi: 10.1016/S0306-4565(03)00005-6 Google Scholar
  213. Scantlebury M, Lovegrove BG, Jackson CR, Bennett NC, Lutermann H (2008) Hibernation and non-shivering thermogenesis in the Hottentot golden mole (Amblysomus hottentottus longiceps). J Comp Physiol B 178:887–897. doi: 10.1007/s00360-008-0277-5 PubMedGoogle Scholar
  214. Scholander PF, Walters V, Hock R, Irving L (1950) Body insulation of some arctic and tropical mammals and birds. Biol Bull 99:225–236PubMedGoogle Scholar
  215. Scholl P (1974) Temperaturregulation beim madegassischen Igeltanrek Echinops telfairi (Martin, 1838). J Comp Physiol B 89:175–195Google Scholar
  216. Schulz TJ, Huang P, Huang TL, Xue R, McDougall LE, Townsend KL, Cypess AM, Mishina Y, Gussoni E, Tseng YH (2013) Brown-fat paucity due to impaired BMP signalling induces compensatory browning of white fat. Nature 495:379–383. doi: 10.1038/nature11943 PubMedCentralPubMedGoogle Scholar
  217. Shabalina IG, Jacobsson A, Cannon B, Nedergaard J (2004) Native UCP1 displays simple competitive kinetics between the regulators purine nucleotides and fatty acids. J Biol Chem 279:38236–38248. doi: 10.1074/jbc.M402375200 PubMedGoogle Scholar
  218. Shabalina IG, Petrovic N, de Jong JMA, Kalinovich AV, Cannon B, Nedergaard J (2013) UCP1 in brite/beige adipose tissue mitochondria is functionally thermogenic. Cell Rep 5:1196–1203. doi: 10.1016/j.celrep.2013.10.044 PubMedGoogle Scholar
  219. Smith BK, Dawson TJ (1984) Changes in the thermal balance of a marsupial (Dasyuroides byrnei) during cold and warm acclimation. J Therm Biol 9:199–204. doi: 10.1016/0306-4565(84)90022-6 Google Scholar
  220. Smith R, Hock R (1963) Brown fat: thermogenic effector of arousal in hibernators. Science 140:199–200PubMedGoogle Scholar
  221. Smith B, Horwitz R (1969) Brown fat and thermogenesis. Physiol Rev 49:330–425PubMedGoogle Scholar
  222. Smith R, Roberts J (1964) Thermogenesis of brown adipose tissue in cold-acclimated rats. Am J Physiol 206:143–148PubMedGoogle Scholar
  223. Sparti A (1992) Thermogenic sapacity of shrews (Mammalia, Soricidae) and its relationship with basal rate of metabolism. Physiol Zool 65:77–96. doi: 10.2307/30158240 Google Scholar
  224. Springer MS, Cleven GC, Madsen O, de Jong WW, Waddell VG, Amrine HM, Stanhope MJ (1997) Endemic African mammals shake the phylogenetic tree. Nature 388:61–64. doi: 10.1038/40386 PubMedGoogle Scholar
  225. Stearns S (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  226. Stier A, Bize P, Habold C, Bouillaud F, Massemin S, Criscuolo F (2014) Mitochondrial uncoupling prevents cold-induced oxidative stress: a case study using UCP1 knockout mice. J Exp Biol 217:624–630. doi: 10.1242/jeb.092700 PubMedGoogle Scholar
  227. Sundin U, Herron D, Cannon B (1981) Brown fat thermoregulation in developing hamsters (Mesocricetus auratus): a GDP-binding study. Biol Neonate 39:142–149PubMedGoogle Scholar
  228. Sundin U, Moore G, Nedergaard J, Cannon B (1987) Thermogenin amount and activity in hamster brown fat mitochondria: effect of cold acclimation. Am J Physiol 252:822–832Google Scholar
  229. Symonds ME, Andrews DC, Buss DS et al (1996) Effect of rearing temperature on perirenal adipose tissue development and thermoregulation following methimazole treatment of postnatal lambs. Exp Physiol 81:995–1006PubMedGoogle Scholar
  230. Thompson GE, Jenkinson DM (1969) Nonshivering thermogenesis in the newborn lamb. Can J Physiol Pharmacol 47:249–253PubMedGoogle Scholar
  231. Thundathil JC, Rajamanickam GD, Kastelic JP, Newton LD (2012) The effects of increased testicular temperature on testis-specific isoform of Na+/K+-ATPase in sperm and its role in spermatogenesis and sperm function. Reprod Domest Anim 47:170–177. doi: 10.1111/j.1439-0531.2012.02072.x PubMedGoogle Scholar
  232. Tine M, Kuhl H, Jastroch M, Reinhardt R (2012) Genomic characterization of the European sea bass Dicentrarchus labrax reveals the presence of a novel uncoupling protein (UCP) gene family member in the teleost fish lineage. BMC Evol Biol 12:62. doi: 10.1186/1471-2148-12-62 PubMedCentralPubMedGoogle Scholar
  233. Trayhurn P (1983) Decreased capacity for non-shivering thermogenesis during lactation in mice. Pflügers Arch 398:264–265. doi: 10.1007/BF00657164 PubMedGoogle Scholar
  234. Trayhurn P, Wusteman MC (1987) Sympathetic activity in brown adipose tissue in lactating mice. Am J Physiol 253:515–520Google Scholar
  235. Trayhurn P, Douglas JB, McGuckin MM (1982) Brown adipose tissue thermogenesis is “suppressed” during lactation in mice. Nature 298:59–60PubMedGoogle Scholar
  236. Trayhurn P, Temple NJ, Van Aerde J (1989) Evidence from immunoblotting studies on uncoupling protein that brown adipose tissue is not present in the domestic pig. Can J Physiol Pharmacol 67:1480–1485PubMedGoogle Scholar
  237. Trzcionka M, Withers KW, Klingenspor M, Jastroch M (2008) The effects of fasting and cold exposure on metabolic rate and mitochondrial proton leak in liver and skeletal muscle of an amphibian, the cane toad Bufo marinus. J Exp Biol 211:1911–1918. doi: 10.1242/jeb.016519 PubMedGoogle Scholar
  238. Ussar S, Lee KY, Dankel SN, Boucher J, Haering MF, Kleinridders A, Thomou T, Xue R, Macotela Y, Cypess AM, Tseng YH, Mellgren G, Kahn CR (2014) ASC-1, PAT2, and P2RX5 are cell surface markers for white, beige, and brown adipocytes. Sci Transl Med 6:247ra103. doi: 10.1126/scitranslmed.3008490
  239. Van der Lans AAJJ, Wierts R, Vosselman MJ, Schrauwen P, Brans B, van Marken Lichtenbelt WD (2014) Cold-activated brown adipose tissue in human adults: methodological issues. Am J Physiol Regul Integr Comp Physiol 307:R103–R113. doi: 10.1152/ajpregu.00021.2014 PubMedGoogle Scholar
  240. Van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JMAFL, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJJ (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500–1508. doi: 10.1056/NEJMoa0808718 PubMedGoogle Scholar
  241. Vatnick I, Tyzbir RS, Welch JG, Hooper AP (1987) Regression of brown adipose tissue mitochondrial function and structure in neonatal goats. Am J Physiol 252:391–395Google Scholar
  242. Vaughan T, Ryan J, Czaplewski N (2000) Mammalogy, 4th edn. Saunders College PublishingGoogle Scholar
  243. Vianna CR, Hagen T, Zhang CY, Bachman E, Boss O, Gereben B, Moriscot AS, Lowell BB, Bicudo JE, Bianco AC (2001) Cloning and functional characterization of an uncoupling protein homolog in hummingbirds. Physiol Genomics 5:137–145PubMedGoogle Scholar
  244. Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, Taittonen M, Laine J, Savisto NJ, Enerbäck S, Nuutila P (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518–1525. doi: 10.1056/NEJMoa0808949 PubMedGoogle Scholar
  245. Wang D, Sun R, Wang Z, Liu J (1999) Effects of temperature and photoperiod on thermogenesis in plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus). J Comp Physiol B 169:77–83PubMedGoogle Scholar
  246. Warnecke L, Geiser F (2010) The energetics of basking behaviour and torpor in a small marsupial exposed to simulated natural conditions. J Comp Physiol B 180:437–445. doi: 10.1007/s00360-009-0417-6 PubMedGoogle Scholar
  247. Warnecke L, Turner JM, Geiser F (2008) Torpor and basking in a small arid zone marsupial. Naturwissenschaften 95:73–78. doi: 10.1007/s00114-007-0293-4 PubMedGoogle Scholar
  248. Warren WC, Hillier LW, Marshall GJ, Birney E, Ponting CP, Grützner F, Belov K, Miller W, Clarke L, Chinwalla AT, Yang SP, Heger A, Locke DP, Miethke P, Waters PD, Veyrunes F, Fulton L, Fulton B, Graves T, Wallis J et al (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature 453:175–183. doi: 10.1038/nature06936 PubMedCentralPubMedGoogle Scholar
  249. Webster AJF, Heitman JH, Hays FL, Olynyk GP (1969) Catecholamines and cold thermogenesis in sheep. Can J Physiol Pharmacol 47:719–724. doi: 10.1139/y69-122 PubMedGoogle Scholar
  250. Woodley R, Buffenstein R (2002) Thermogenic changes with chronic cold exposure in the naked mole-rat (Heterocephalus glaber). Comp Biochem Physiol A Mol Integr Physiol 133:827–834PubMedGoogle Scholar
  251. Wu J, Boström P, Sparks LM, Ye L, Choi JH, Giang AH, Khandekar M, Virtanen KA, Nuutila P, Schaart G, Huang K, Tu H, van Marken Lichtenbelt WD, Hoeks J, Enerbäck S, Schrauwen P, Spiegelman BM (2012) Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 150:366–376. doi: 10.1016/j.cell.2012.05.016 PubMedCentralPubMedGoogle Scholar
  252. Wu J, Cohen P, Spiegelman BM (2013) Adaptive thermogenesis in adipocytes : is beige the new brown? Genes Dev 27:234–250. doi: 10.1101/gad.211649.112.from PubMedCentralPubMedGoogle Scholar
  253. Wunder B (1984) Strategies for, and environmental cueing mechanisms of, seasonal changes in thermoregulatory parameters of small mammals. In: Merrit J (ed) Winter ecology of small mammals. Carnegie Museum of Natural History special publication, Pittsburgh, pp 165–172Google Scholar
  254. Xue B, Coulter A, Rim JS, Koza RA, Kozak LP (2005) Transcriptional synergy and the regulation of Ucp1 during brown adipocyte induction in white fat depots. Mol Cell Biol 25:8311–8322. doi: 10.1128/MCB.25.18.8311-8322.2005 PubMedCentralPubMedGoogle Scholar
  255. Xue B, Rim J-S, Hogan JC, Coulter AA, Koza RA, Kozak LP (2007) Genetic variability affects the development of brown adipocytes in white fat but not in interscapular brown fat. J Lipid Res 48:41–51PubMedGoogle Scholar
  256. Yang DB, Li L, Wang LP, Chi QS, Hambly C, Wang DH, Speakman JR (2013) Limits to sustained energy intake. XIX. A test of the heat dissipation limitation hypothesis in Mongolian gerbils (Meriones unguiculatus). J Exp Biol 216:3358–3368. doi: 10.1242/jeb.085233 PubMedGoogle Scholar
  257. Ye JM, Edwards SJ, Rose RW, Steen JT, Clark MG, Colquhoun EQ (1996) Alpha-adrenergic stimulation of thermogenesis in a rat kangaroo (Marsupialia, Bettongia gaimardi). Am J Physiol 271:586–592Google Scholar
  258. Young P, Arch JR, Ashwell M (1984) Brown adipose tissue in the parametrial fat pad of the mouse. FEBS Lett 167:10–14PubMedGoogle Scholar
  259. Zegers D, Merrit J (1988) Effect of photoperiod and ambient temperature on non-shivering thermogenesis of Peromyscus maniculatus. Acta Theriol 33:273–281Google Scholar
  260. Zeisberger E, Brück K (1967) Quantitative Beziehungen zwischen Noradrenalin-Effekt und Ausmaß der zitterfreien Thermogenese beim Meerschweinchen. Pflügers Arch ges Physiol 296:263–275Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • R. Oelkrug
    • 1
    • 4
  • E. T. Polymeropoulos
    • 2
  • M. Jastroch
    • 3
  1. 1.Department of Animal Physiology, Faculty of BiologyPhilipps-Universität MarburgMarburgGermany
  2. 2.CSIRO Marine and Atmospheric Research, Food Futures FlagshipHobartAustralia
  3. 3.Institute for Diabetes and Obesity, Helmholtz Zentrum München, German Research Center for Environmental Health (GmbH)MunichGermany
  4. 4.Institute of Pharmacology and Toxicology, Biomedical CenterUniversity of BonnBonnGermany

Personalised recommendations