Успехи современной биологии, 2023, T. 143, № 4, стр. 375-392

Преадаптивность несократительного термогенеза в эволюции теплокровности у позвоночных

В. А. Черлин *

Дагестанский государственный университет
Махачкала, Республика Дагестан, Россия

* E-mail: cherlin51@mail.ru

Поступила в редакцию 04.03.2023
После доработки 19.04.2023
Принята к публикации 19.04.2023

Аннотация

Большая часть тепла, которая выделяется в организме позвоночных, производится в мышцах при сократительном (во время движения или дрожания) и несократительном (без мышечной активности) термогенезе. Сократительный термогенез характерен для всех позвоночных, но он не способен постоянно поддерживать у животных высокую температуру тела. Основная идея, рассмотренная в данной статье и базирующаяся на уже большом количестве публикаций последних лет: главная биохимическая база теплокровности у позвоночных – часть цикла сокращения–расслабления поперечнополосатой скелетной мускулатуры, в котором акт сокращения мышц тем или иным образом выпадает, а энергия, которая должна была быть на это затрачена, рассеивается в виде теплоты. Этот несократительный термогенез, который способен поддерживать региональную и общую эндотермию позвоночных, и можно считать реальной биохимической основой теплокровности. Таким образом, наличие скелетной мускулатуры у всех позвоночных и общие биохимические основы цикла сокращения–расслабления представляют собой единое преадаптивное свойство проявления несократительного термогенеза у всех позвоночных, начиная с рыб, что является базой для эволюции теплокровности. Поэтому вполне объяснимы и неудивительны современные данные о том, что первые наземные позвоночные, скорее всего, были животными с высокими уровнями и метаболизма, и температуры тела.

Ключевые слова: биохимия несократительного термогенеза, теплокровность, эволюция теплокровности

Список литературы

  1. Орлов Н.Л. Факультативная эндогенная терморегуляция питонов (Boidae, Pythoninae) и корреляция между эндотермными реакциями и поведенческой терморегуляцией // Зоол. журн. 1986. Т. 65. С. 551–559.

  2. Проссер Л. Сравнительная физиология животных. Т. 1. М.: Мир, 1977. 609 с.

  3. Трошин А.С., Трошина В.П. Физиология клетки. М.: Просвещение, 1978. 119 с.

  4. Черлин В.А. Гипотеза о механизмах эволюционного процесса и его канализации на примере позвоночных животных. 1. Эволюция, связанная с высокой температурой тела // Успехи соврем. биол. 2021а. Т. 141 (1). С. 78–104.

  5. Черлин В.А. Гипотеза о механизмах эволюционного процесса и его канализации на примере позвоночных животных. 2. Некоторые механизмы эволюционного процесса у позвоночных // Успехи соврем. биол. 2021б. Т. 141 (2). С. 189–208.

  6. Черлин В.А. Эволюция термобиологических статусов у позвоночных животных. 1. Температуры тела вымерших и современных рептилий // Журн. общ. биол. 2021в. Т. 82 (6). С. 445–458.

  7. Черлин В.А. Эволюция термобиологических статусов у позвоночных животных. 2. Развитие отношений с температурой у позвоночных животных // Журн. общ. биол. 2021г. Т. 82 (6). С. 459–477.

  8. Четанов Н.А., Литвинов Н.А., Югов М.В. Влияние температуры на интенсивность метаболизма у двух видов круглоголовок // Изв. Самар. науч. центра РАН. 2014. Т. 16. № 5 (1). С. 445–447.

  9. Anderson K. Multi-omic analysis of hibernator skeletal muscle and calcium handling regulation. Th. … M.S. Minnesota: Univ. of Minnesota, 2016. 67 p.

  10. Arruda A.P., Ketzer L.A., Nigro M. et al. Cold tolerance in hypothyroid rabbits: role of skeletal muscle mitochondria and sarcoplasmic reticulum Ca2+ ATPase isoform 1 heat production // Endocrinology. 2008. V. 149. P. 6262–6271.

  11. Augee M.L. Monotremes and the evolution of homeothermy // Monotreme biology / Ed. M.L. Augee. Sydney: R. Zool. Soc. N.S.W., 1978. P. 111–120.

  12. Augee M.L., Gooden B., Musser A. Echidna: extraordinary egg-laying mammal. Clayton: CSIRO Publ., 2006. 136 p.

  13. Bal N.C., Maurya S.K., Sopariwala D.H. et al. Sarcolipin is a newly identified regulator of muscle-based thermogenesis in mammals // Nat. Med. 2012. V. 18. P. 1575–1579.

  14. Bal N.C., Maurya S.K., Singh S. et al. Increased reliance on muscle-based thermogenesis upon acute minimization of brown adipose tissue function // J. Biol. Chem. 2016. V. 291. P. 17247–17257.

  15. Bal N.C., Maurya S.K., Pani S. et al. Mild cold induced thermogenesis: are BAT and skeletal muscle synergistic partners? // Biosci. Rep. 2017. V. 37. P. BSR20171087.

  16. Bal N.C., Sahoo S.K., Maurya S.K., Periasamy M. The role of sarcolipin in muscle nonshivering thermogenesis // Front. Physiol. 2018. V. 9. P. 1217. https://doi.org/10.3389/fphys.2018.01217

  17. Bal N.C., Gupta S.C., Pan M. et al. Is upregulation of sarcolipin beneficial or detrimental to muscle function? // Front. Physiol. 2021. V. 12. P. 633058.

  18. Barré H., Nedergaard J. Cold-induced changes in Ca2+ transport in duckling skeletal muscle mitochondria // Am. J. Physiol. 1987. V. 252. P. R1046–R1054.

  19. Barré H., Duchamp C., Rouanet J.-L. et al. Muscular nonshivering thermogenesis in cold-acclimated ducklings // Physiology of cold adaptation in birds / Eds C. Bech, R.E. Reinertsen. N.Y.: Plenum, 1989. P. 49–58.

  20. Bartholomew G.A. Physiological control of body temperature // Biology of the Reptilia. V. 12. Physiology C – Physiological Ecology / Eds C. Gans, F.H. Pough. N.Y.: Acad. Press, 1982. P. 167–211.

  21. Benedict F.G. The physiology of large reptiles with special reference to the heat production of snakes, tortoises, lizards and alligators. Washington: Carnegie Inst., 1932. 539 p.

  22. Bernal D., Donley J.M., Shadwick R.E., Syme D.A. Mammal-like muscles power swimming in a cold-water shark // Nature. 2005. V. 437. P. 1349–1352.

  23. Bicudo J.E., Vianna C.R., Chaui-Berlinck J.G. Thermogenesis in birds // Biosci. Rep. 2001. V. 21. P. 181–188.

  24. Bicudo J.E., Bianco A.C., Vianna C.R. Adaptive thermogenesis in hummingbirds // J. Exp. Biol. 2002. V. 205. P. 2267–2273.

  25. Blank J.M., Morrissette J.M., Farwell C.J. et al. Temperature effects on metabolic rate of juvenile Pacific bluefin tuna Thunnus orientalis // J. Exp. Biol. 2007. V. 210. P. 4254–4261.

  26. Blix A.S. Adaptations to polar life in mammals and birds // J. Exp. Biol. 2016. V. 219. P. 1093–1105.

  27. Block B.A. Thermogenesis in muscle // Ann. Rev. Physiol. 1994. V. 56. P. 535–577.

  28. Bostrom B.L., Jones T.T., Hastings M., Jones D.R. Behaviour and physiology: the thermal strategy of leatherback turtles // PLoS One. 2010. V. 5. Art. e13925.

  29. Brattstrom B.H., Collins R. Thermoregulation // Int. Turtle Tortoise Soc. J. 1972. V. 16 (5). P. 15–19.

  30. Brigham R.M., Trayhurn P. Brown fat in birds? A test for the mammalian BAT-specific mitochondrial uncoupling protein in common poorwills // Condor. 1994. V. 96. P. 208–211.

  31. Bruton J.D., Aydin J., Yamada T. et al. Increased fatigue resistance linked to Ca2+-stimulated mitochondrial biogenesis in muscle fibres of cold-acclimated mice // J. Physiol. 2010. V. 588. P. 4275–4288.

  32. Bundle M.W., Hansen K.S., Dial K.P. Does the metabolic rate-flight speed relationship vary among geometrically similar birds of different mass? // J. Exp. Physiol. 2007. V. 210. P. 1075–1083.

  33. Burness G., Diamond J., Flannery T. Dinosaurs, dragons, and dwarfs: the evolution of maximal body size // PNAS USA. 2001. V. 98. P. 14518–14523.

  34. Cannon B., Nedergaard J. Brown adipose tissue: function and physiological significance // Physiol. Rev. 2004. V. 84. P. 277–359.

  35. Cannon B., Golozoubova V., Matthias A. et al. Is there life in the cold without UCP1? Uncoupling proteins and thermoregulatory thermogenesis // Life in the cold / Eds G. Heldmaier, M. Klingenspor. 11th Int. Hibernat. Symp. (Jungholz, August 13–18, 2000). Berlin: Springer, 2000. P. 387–400.

  36. Carey F.G., Teal J.M. Heat conservation in tuna fish muscle // PNAS USA. 1966. V. 56. P. 1464–1469.

  37. Carey F.G., Teal J.M. Mako and porbeagle: warm-bodied sharks // Com. Biochem. Physiol. 1969. V. 28. P. 199–204.

  38. Chaffee R.R., Roberts J.C. Temperature acclimation in birds and mammals // Annu. Rev. Physiol. 1971. V. 33. P. 155–202.

  39. Cheah K.S., Dauncey M.J., Cheah A.M., Ingram D.L. Influence of environmental temperature and energy intake on porcine skeletal muscle mitochondria // Comp. Biochem. Physiol. 1985. V. 82. P. 287–292.

  40. Ciezarek A.G., Osborne O.G., Shipley O.N. et al. Phylotranscriptomic insights into the diversification of endothermic Thunnus tunas // Mol. Biol. Evol. 2019. V. 36. P. 84–96.

  41. Cloudsley-Thompson J.L. Physiological thermoregulation in the spurred tortoise (Testudo graeca) // J. Natur. Hist. 1974. V. 8 (5). P. 577–587.

  42. Crawshaw L.I., Moffitt B.P., Lemons D.E., Downey J.A. The evolutionary development of vertebrate thermoregulation // Am. Sci. 1981. V. 69 (5). P. 543–550.

  43. Da Costa D.C., Landeira-Fernandez A.M. Thermogenic activity of the Ca2+-ATPase from blue marlin heater organ: regulation by KCl and temperature // Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009. V. 297. R1460–R1468.

  44. Davenport J., Fraher J., Fitzgerald E. et al. Fat head: an analysis of head and neck insulation in the leatherback turtle (Dermochelys coriacea) // J. Exp. Biol. 2009. V. 212. P. 2753–2759.

  45. Davenport J., Jones T.T., Work T.M., Balazs G.H. Topsy-turvy: turning the counter-current heat exchange of leatherback turtles upside down // Biol. Lett. 2015. V. 11. P. e20150592.

  46. Davesne D., Gueriau P., Dutheil D.B., Bertrand L. Exceptional preservation of a Cretaceous intestine provides a glimpse of the early ecological diversity of spiny-rayed fishes (Acanthomorpha, Teleostei) // Sci. Rep. 2018. V. 8. P. 8509.

  47. Dawson W.R., Templeton J.R. Physiological responses to temperature in the alligator lizard, Gerrhonotus multicarinatus // Ecology. 1966. V. 47. P. 759–765.

  48. Dawson T.J. Responses to cold of monotremes and marsupials // Animal adaptation to cold. Advances in comparative and environmental physiology. V. 4 / Eds L.C.H. Wang, R.J. Brooks, J.A. Boulant. Berlin, Heidelberg: Springer, 1989. P. 255–288.

  49. Dawson W.R., Carey C. Seasonal acclimatization to temperature in cardueline finches // J. Comp. Physiol. 1976. V. 112 (3). P. 317–333.

  50. De Andrade D.V. Temperature effects on the metabolism of amphibians and reptiles: caveats and recommendations // Amphibian and reptile adaptations to the environment: interplay between physiology and behavior / Eds D.V. De Andrade, C.R. Bevier, J.E. De Carvalho. San Diego: CRC Press, 2016. P. 129–154.

  51. De Andrade D.V., Brito S.P., Toledo L.F., Abe A.S. Seasonal changes in blood oxygen transport and acid-base status in the tegu lizard, Tupinambis merianae // Respir. Physiol. Neurobiol. 2004. V. 140. P. 197–208.

  52. De Bruijn R., Romero L.M. Behavioral and physiological responses of wild-caught European starlings (Sturnus vulgaris) to a minor, rapid change in ambient temperature // Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2011. V. 160. P. 260–266.

  53. Duchamp C., Barré H. Skeletal muscle as the major site of nonshivering thermogenesis in cold-acclimated ducklings // Am. J. Physiol. 1993. V. 265. P. R1076–R1083.

  54. Duchamp C., Barré H., Rouanet J.L. et al. Nonshivering thermogenesis in king penguin chicks. I. Role of skeletal muscle // Am. J. Physiol. 1991. V. 261. P. R1438–R1445.

  55. Dumonteil E., Barré H., Meissner G. Sarcoplasmic reticulum Ca(2+)-ATPase and ryanodine receptor in cold-acclimated ducklings and thermogenesis // Am. J. Physiol. 1993. V. 265. P. C507–C513.

  56. Dumonteil E., Barré H., Meissner G. Expression of sarcoplasmic reticulum Ca2+ transport proteins in cold-acclimating ducklings // Am. J. Physiol. 1995. V. 269. P. C955–C960.

  57. Dunlap D.G. Influence of temperature and duration of acclimation, time of day, sex and body weight on metabolic rates in the hylid frog, Acris crepitans // Comp. Biochem. Physiol. 1969. V. 31. P. 555–570.

  58. Dutton R.H., Fitzpatrick L.C. Metabolic compensation to seasonal temperatures in the rusty lizard, Sceloporus olivaceus // Comp. Biochem. Physiol. A. 1975. V. 51. P. 309–318.

  59. Eldershaw T.P.D., Ye J., Clarke M.J., Colquhoun E.Q. Vasoconstrictor-induced thermogenic switching in ectotherm and endotherm muscle // Adaptations to the cold / Eds F. Geiser, A.J. Hulbert, S.C. Nicol. 10th Int. Hibernat. Symp. (Tasmania, 30 June–6 July, 1996) Armidale: Univ. N. Eng. Press, 1996. P. 311–317.

  60. Emre Y., Hurtaud C., Ricquier D. et al. Avian UCP: the killjoy in the evolution of the mitochondrial uncoupling proteins // J. Mol. Evol. 2007. V. 65. P. 392–402.

  61. Engbretson G.A., Livezey R.L. The effects of aggressive display on body temperature in the fence lizard Sceleporus occidentalis occidentalis Baird and Girard // Physiol. Biochem. Zool. 1972. V. 45. P. 247–254.

  62. Estefa J., Klembara J., Tafforeau P., Sanchez S. Limb-bone development of seymouriamorphs: implications for the evolution of growth strategy in stem amniotes // Front. Earth Sci. 2020. V. 8. Art. 97. P. 1–21.

  63. Fair W., Ackman R.G., Mrosovsky N. Body temperature of Dermochelys coriacea: warm turtle from cold water // Science. 1972. V. 177. P. 791–793.

  64. Filali-Zegzouti Y., Abdelmelek H., Rouanet J.L. et al. Role of catecholamines in glucagon-induced thermogenesis // J. Neural. Transm. 2005. V. 112. P. 481–489.

  65. Franck J.P.C., Slight-Simcoe E., Wegner N.C. Endothermy in the smalleye opah (Lampris incognitus): a potential role for the uncoupling protein sarcolipin // Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2019. V. 233. P. 48–52.

  66. Fyda T.J., Spencer C., Jastroch M., Gaudry M. Disruption of thermogenic UCP1 predated the divergence of pigs and peccaries // J. Exp. Biol. 2020. V. 223. P. jeb223974. https://doi.org/10.1242/jeb.223974

  67. Galvao P.E., Tarasantchi J., Guertzenstein P. Heat production of tropical snakes // Am. J. Physiol. 1965. V. 209. P. 501–506.

  68. Gaudry M.J., Jastroch M., Treberg J.R. et al. Inactivation of thermogenic UCP1 as a historical contingency in multiple placental mammal clades // Sci. Adv. 2017. V. 3. P. e1602878.

  69. Gaudry M.J., Campbell K.L., Jastroch M. Evolution of UCP1 // Brown adipose tissue / Eds A. Pfeifer, M. Kingenspor, S. Herzig. Cham: Springer, 2018. P. 127–141.

  70. Geiser F. Daily torpor and thermoregulation in Antechinus (Marsupialia): influence of body mass, season, development, reproduction, and sex // Oecologia. 1988. V. 77. P. 395–399.

  71. Geiser F., Körtner G. Hibernation and daily torpor in Australian mammals // Austr. Zool. 2010. V. 35. P. 204–215.

  72. Grav H.J., Borch-Iohnsen B., Dahl H.A. et al. Oxidative capacity of tissues contributing to thermogenesis in eider (Somateria mollissima) ducklings: changes associated with hatching // J. Comp. Physiol. B. 1988. V. 158. P. 513–518.

  73. Greenway D.C., Himms-Hagen J. Increased calcium uptake by muscle mitochondria of cold-acclimated rats // Am. J. Physiol. 1978. V. 234. P. C7–C13.

  74. Greer A.E., Lazell J.D., Wright R.M. Anatomical evidence for a counter-current heat exchanger in the leatherback turtle (Dermochelys coriacea) // Nature. 1973. V. 244. P. 181.

  75. Grigg G.C. An evolutionary framework for studies of hibernation and shortterm torpor // Life in the cold / Eds B.M. Barnes, H.V. Carey. 12th Int. Hibernat. Symp. (Vancouver, 25 July–1 August, 2004). Fairbanks: Institute of Arctic Biology, University of Alaska, 2004. P. 131–141.

  76. Grigg G.C., Beard L. Hibernation by echidnas in mild climates: hints about the evolution of endothermy? // Life in the cold / Eds G. Heldmaier, M. Klingenspor. 11th Int. Hibernat. Symp. (Jungholz, August 13–18, 2000). Berlin: Springer, 2000. P. 5–20.

  77. Grigg G.C., Beard L.A., Augee M.L. Hibernation in a monotreme, the echidna (Tachyglossus aculeatus) // Comp. Biochem. Physiol. A Comp. Physiol. 1989. V. 92. P. 609–612.

  78. Grigg G.C., Augee M., Beard L. Thermal relations of free-living echidnas during activity and in hibernation in a cold climate // Platypus and echidnas / Ed. M.L. Augee. Mosman: R. Zool. Soc. N.S.W., 1992. P. 160–173.

  79. Grigg G.C., Beard L.A., Augee M.L. The evolution of endothermy and its diversity in mammals and birds // Physiol. Biochem. Zool. 2004. V. 77. P. 982–997.

  80. Grigg G., Nowack J., Bicudo J.E.P.W. et al. Whole-body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians // Biol. Rev. Camb. Philos. Soc. 2022. V. 97. P. 766–801.

  81. Guglielmo C.G. Move that fatty acid: fuel selection and transport in migratory birds and bats // Integr. Comp. Biol. 2010. V. 50. P. 336–345.

  82. Haman F., Blondin D.P. Shivering thermogenesis in humans: origin, contribution and metabolic requirement // Temperature. 2017. V. 4. P. 217–226.

  83. Harlow P., Grigg G. Shivering thermogenesis the production of heat, especially within the animal body thermogenesis in brooding diamond python, Python spilotes spilotes // Copeia. 1984. V. 4. P. 959–965.

  84. Hashimoto Y., Nishimura T., Kurobe Y. et al. Effect of 3',5'-dimethylpyrazole on colonic temperature, plasma glucose, NEFA and corticosterone in the non-acclimated rats subjected to cold // Jpn. J. Pharm. 1970. V. 20. P. 441–442.

  85. Hayward J.S., Lisson P.A. Evolution of brown fat: its absence in marsupials and monotremes // Can. J. Zool. 1992. V. 70. P. 171–179.

  86. Hirabayashi M., Ijiri D., Kamei Y. et al. Transformation of skeletal muscle from fast- to slow-twitch during acquisition of cold tolerance in the chick // Endocrinology. 2005. V. 146. P. 399–405.

  87. Holloway J.C., Geiser F. Seasonal changes in the thermoenergetics of the marsupial sugar glider, Petaurus breviceps // J. Com. Physiol. 2001. V. 171. P. 643–650.

  88. Hudson J.W., Bertram F.W. Physiological responses to temperature in the ground skink, Lygosoma laterale // Physiol. Zool. 1966. V. 39. P. 21–29.

  89. Hudson D.M., Bernstein M.H. Gas exchange and energy cost of flight in the white-necked raven, Corvus cryptoleucus // J. Experim. Biol. 1983. V. 103. P. 121–130.

  90. Huey R.B. Temperature, physiology and the ecology of reptiles // Biology of the reptilia. V. 12 / Ed. C. Gans. L.: Acad. Press, 1982. P. 25–92.

  91. Huey R.B., Slatkin M. Cost and benefits of lizard thermoregulation // Q. Rev. Biol. 1976. V. 51. P. 363–384.

  92. Hutchison V.H., Dowling H.D., Vinegar A. Thermoregulation in a brooding female Indian python, Python molurus bivittatus // Science. 1966. V. 151. P. 694–696.

  93. Ijiri D., Miura M., Kanai Y., Hirabayashi M. Increased mass of slow-type skeletal muscles and depressed myostatin gene expression in cold-tolerant chicks // Zool. Sci. 2009. V. 26. P. 277–283.

  94. Jastroch M., Withers K.W., Stoehr S., Klingenspor M. Mitochondrial proton conductance in skeletal muscle of a cold-exposed marsupial, Antechinus flavipes, is unlikely to be involved in adaptive nonshivering thermogenesis but displays increased sensitivity toward carbon-centered radicals // Physiol. Biochem. Zool. 2009. V. 82. P. 447–454.

  95. Jastroch M., Oelkrug R., Keipert S. Insights into brown adipose tissue evolution and function from non-model organisms // J. Exp. Biol. 2018. V. 221. P. jeb169425.

  96. Jenni L., Jenni-Eiermann S. Fuel supply and metabolic constraints in migrating birds // J. Avian Biol. 1998. V. 29. P. 521–528.

  97. Johnson C.R. Thermoregulation in crocodilians. I. Headbody temperature control in the papuan-New Guinean crocodiles, Crocodilus novoaguineae and Crocodilus porosus // Comp. Biochem. Physiol. A Comp. Physiol. 1974. V. 49 (1). P. 3–28.

  98. Johnston D.W. The absence of brown adipose tissue in birds // Comp. Biochem. Physiol. A Com. Physiol. 1971. V. 40. P. 1107–1108.

  99. Kabat A.P., Rose R.W., Harris J., West A.K. Molecular identification of uncoupling proteins (UCP2 and UCP3) and absence of UCP1 in the marsupial Tasmanian bettong, Bettongia gaimardi // Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2003a. V. 134. P. 71–77.

  100. Kabat A.P., Rose R.W., West A.K. Nonshivering thermogenesis in a carnivorous marsupial, Sarcophilus harrisii, in the absence of UCP1 // J. Therm. Biol. V. 28. 2003b. P. 413–420.

  101. Kaspari R.R., Reyna-Neyra A., Jung L. et al. The paradoxical lean phenotype of hypothyroid mice is marked by increased adaptive thermogenesis in the skeletal muscle // PNAS USA. 2020. V. 117. P. 22545–22551.

  102. Klingenberg M. The ADP and ATP transport in mitochondria and its carrier // Biochim. Biophys. Acta. 2008. V. 1778. P. 1978–2021.

  103. Kohler M., Marin-Moratalla N., Jordana X., Aanes R. Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology // Nature. 2012. V. 487. P. 358–361.

  104. Kunji E.R., Aleksandrova A., King M.S. et al. The transport mechanism of the mitochondrial ADP/ATP carrier // Biochim. Biophys. Acta. 2016. V. 1863. P. 2379–2393.

  105. Lamarre-Picquot P. Troisieme memoirs sur l’incubation et quatre phenomenes observes ches les ophidiens. Paris: Comp. Rend., Acad. Sci., 1842. V. 14. P. 164.

  106. Legendre L.J., Davesne D. The evolution of mechanisms involved in vertebrate endothermy // Phil. Trans. R. Soc. B. 2020. V. 375 (1793). P. e20190136.

  107. Marmonier F., Duchamp C., Cohen-Adad F. et al. Hormonal control of thermogenesis in perfused muscle of muscovy ducklings // Am. J. Physiol. 1997. V. 273. P. R1638–R1648.

  108. Matoba H., Murakami N. Histochemical changes of rat skeletal muscles induced by cold acclimation // Jpn. J. Physiol. 1981. V. 31. P. 273–278.

  109. Maurya S.K., Herrera J.L., Sahoo S.K. et al. Sarcolipin signaling promotes mitochondrial biogenesis and oxidative metabolism in skeletal muscle // Cell Rep. 2018. V. 24. P. 2919–2931.

  110. Mollica M.P., Lionetti L., Crescenzo R. et al. Cold exposure differently influences mitochondrial energy efficiency in rat liver and skeletal muscle // FEBS Lett. 2005. V. 579. P. 1978–1982.

  111. Montigny C., Decottignies P., Le Marechal P. et al. S-palmitoylation and s-oleoylation of rabbit and pig sarcolipin // J. Biol. Chem. 2014. V. 289. P. 33850–33861.

  112. Morrissette J.M., Franck J.P., Block B.A. Characterization of ryanodine receptor and Ca2+-ATPase isoforms in the thermogenic heater organ of blue marlin (Makaira nigricans) // J. Exp. Biol. 2003. V. 206. P. 805–812.

  113. Nedergaard J., Cannon B. Brown adipose tissue as a heat-producing thermoeffector // Handb. Clin. Neurol. 2018. V. 156. P. 137–152.

  114. Nicol S.C. Energy homeostasis in monotremes // Front. Neurosci. 2017. V. 11. P. 195.

  115. Nicol S.C., Andersen N.A. Rewarming rates and thermogenesis in hibernating echidnas // Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2008. V. 150. P. 189–195.

  116. Nicolaisen T.S., Klein A.B., Dmytriyeva O. et al. Thyroid hormone receptor α in skeletal muscle is essential for T3-mediated increase in energy expenditure // FASEB J. 2020. V. 34. P. 15480–15491.

  117. Nowack J., Giroud S., Arnold W., Ruf T. Muscle nonshivering thermogenesis and its role in the evolution of endothermy // Front. Physiol. 2017. V. 8. P. 889.

  118. Nowack J., Vetter S.G., Stalder G. et al. Muscle nonshivering thermogenesis in a feral mammal // Sci. Rep. 2019. V. 9. P. 6378.

  119. Oliver S.R., Anderson K.J., Hunstiger M.M., Andrews M.T. Turning down the heat: down-regulation of sarcolipin in a hibernating mammal // Neurosci. Lett. 2019. V. 696. P. 13–19.

  120. Pant M., Bal N.C., Periasamy M. Sarcolipin: a key thermogenic and metabolic regulator in skeletal muscle // Tr. Endocrinol. Metab. 2016. V. 27. P. 881–892.

  121. Paladino F.V., O’Connor M.P., Spotila J.R. Metabolism of leatherback turtles, gigantothermy and thermoregulation of dinosaurs // Nature. 1990. V. 344. P. 858–860.

  122. Pearson O.P., Bradford D.F. Thermoregulation of lizards and toad at high altitudes in Peru // Copeia. 1976. № 1. P. 155–170.

  123. Polymeropoulos E.T., Jastroch M., Frappell P.B. Absence of adaptive nonshivering thermogenesis in a marsupial, the fat-tailed dunnart (Sminthopsis crassicaudata) // J. Comp. Physiol. 2012. V. 182. P. 393–401.

  124. Puigserver P., Wu Z., Park C.W. et al. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis // Cell. 1998. V. 92. P. 829–839.

  125. Raimbault S., Dridi S., Denjean F. et al. An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds // Biochem. J. 2001. V. 353. P. 441–444.

  126. Rey B., Roussel D., Romestaing C. et al. Upregulation of avian uncoupling protein in cold-acclimated and hyperthyroid ducklings prevents reactive oxygen species production by skeletal muscle mitochondria // BMC Physiol. 2010. V. 10. P. 5.

  127. Romer A.S., Parsons T.S. The vertebrate body. Philadelphia: Saunders Co., 1977. 624 p.

  128. Rose R.W., Kuswanti N. Thyroid function and the development of endothermy in a marsupial, the Tasmanian bettong, Bettongia gaimardi (Demarest 1822) // Gen. Comp. Endocrinol. 2004. V. 136. P. 17–22.

  129. Rose R.W., West A.K., Ye J.M. et al. Nonshivering thermogenesis in a marsupial (the Tasmanian bettong, Bettongia gaimardi) is not attributable to brown adipose tissue // Physiol. Biochem. Zool. 1999. V. 72. P. 699–704.

  130. Rothwell N.J., Stock M.J. Biological distribution and significance of brown adipose tissue // Comp. Biochem. Physiol. A Comp. Physiol. 1985. V. 82. P. 745–751.

  131. Rotter D., Peiris H., Grinsfelder D.B. et al. Regulator of calcineurin 1 helps coordinate whole-body metabolism and thermogenesis // EMBO Rep. 2018. V. 19. P. e44706.

  132. Roussel D., Chainer F., Rouanet J.L., Barré H. Increase in the adenine nucleotide translocase content of duckling subsarcolemmal mitochondria during cold acclimation // FEBS Lett. 2000. V. 477. P. 141–144.

  133. Rowland L.A., Bal N.C., Kozak L.P., Periasamy M. Uncoupling protein 1 and sarcolipin are required to maintain optimal thermogenesis, and loss of both systems compromises survival of mice under cold stress // J. Biol. Chem. 2015a. V. 290. P. 12282–12289.

  134. Rowland L.A., Bal N.C., Periasamy M. The role of skeletal-muscle-based thermogenic mechanisms in vertebrate endothermy // Biol. Rev. Camb. Phil. Soc. 2015b. V. 90. P. 1279–1297.

  135. Rowlatt U., Mrosovsky N., English A. A comparative survey of brown fat in the neck and axilla of mammals at birth // Biol. Neonate. 1971. V. 17. P. 53–83.

  136. Rudas P., Pethes G. Studies on the conversion of thyroxine to 3,5,3'-triiodothyronine in normal and thyroidectomized chickens // Gen. Comp. Endocrinol. 1984. V. 54. P. 154–161.

  137. Runcie R.M., Dewar H., Hawn D.R. et al. Evidence for cranial endothermy in the opah (Lampris guttatus) // J. Exp. Biol. 2009. V. 212. P. 461–470.

  138. Ruuskanen S., Hsu B.-Y., Nord A. Endocrinology of thermoregulation in birds in a changing climate // Mol. Cell. Endocrinol. 2021. V. 519. P. 111088.

  139. Saarela S., Keith J.S., Hohtola E., Trayhurn P. Is the “mammalian” brown fat-specific mitochondrial uncoupling protein present in adipose tissues of birds? // Comp. Biochem. Physiol. 1991. V. 100. P. 45–49.

  140. Saito S., Saito C.T., Shingai R. Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals // Gene. 2008. V. 408. P. 37–44.

  141. Sahoo S.K., Shaikh S.A., Sopariwala D.H. et al. The N terminus of sarcolipin plays an important role in uncoupling sarco-endoplasmic reticulum Ca2+-ATPase (SERCA) ATP hydrolysis from Ca2+ transport // J. Biol. Chem. 2015. V. 290. P. 14057–14067.

  142. Sanders C.J., Santos I.R., Maher D.T. et al. Dissolved iron exports from an estuary surrounded by coastal wetlands: can small estuaries be a significant source of Fe to the ocean? // Marine Chem. 2015. V. 176. P. 75–82.

  143. Sapsford C.W., Hughes G.R. Body temperature of the loggerhead sea turtle Caretta caretta and the leatherback sea turtle Dermochelys coriacea during nesting // Zool. Afr. 1978. V. 18 (1). P. 63–69.

  144. Schaeffer P.J., Villarin J.J., Lindstedt S.L. Chronic cold exposure increases skeletal muscle oxidative structure and function in Monodelphis domestica, a marsupial lacking brown adipose tissue // Physiol. Biochem. Zool. 2003. V. 76. P. 877–887.

  145. Schaeffer P.J., Villarin J.J., Pierotti D.J. et al. Cost of transport is increased after cold exposure in Monodelphis domestica: training for inefficiency // J. Exp. Biol. 2005. V. 208. P. 3159–3167.

  146. Schwartz T.S., Murray S., Seebacher F. Novel reptilian uncoupling proteins: molecular evolution and gene expression during cold acclimation // Proc. Biol. Sci. 2008. V. 275. P. 979–985.

  147. Seebacher F., Grigg G.C., Beard L.A. Crocodiles as dinosaurs: behavioural thermoregulation in very large ectotherms leads to high and stable body temperatures // J. Exp. Biol. 1999. V. 202. P. 77–86.

  148. Sepulveda C., Dickson K., Frank L., Graham J. Cranial endothermy and a putative brain heater in the most basal tuna species, Allothunnus fallai // J. Fish Biol. 2007. V. 70. P. 1720–1733.

  149. Sepulveda C., Dickson K., Bernalk D. et al. Elevated red myotomal muscle temperatures in the most basal tuna species, Allothunnus fallai // J. Fish Biol. 2008. V. 73. P. 241–249.

  150. Shabalina I.G., Hoeks J., Kramarova T.V. et al. Cold tolerance of UCP1-ablated mice: a skeletal muscle mitochondria switch toward lipid oxidation with marked UCP3 up-regulation not associated with increased basal, fatty acid- or ROS-induced uncoupling or enhanced GDP effects // Biochim. Biophys. Acta. 2010. V. 1797. P. 968–980.

  151. Silva J.E. Thermogenic mechanisms and their hormonal regulation // Physiol. Rev. 2006. V. 86. P. 435–464.

  152. Simonyan R.A., Jimenez M., Ceddia R.B. et al. Cold-induced changes in the energy coupling and the UCP3 level in rodent skeletal muscles // Biochim. Biophys. Acta. 2001. V. 1505. P. 271–279.

  153. Sirsat S.K., Sirsat T.S., Crossley J.L. et al. The 12-day thermoregulatory metamorphosis of red-winged blackbirds (Agelaius phoeniceus) // J. Comp. Physiol. 2016. V. 186. P. 651–663.

  154. Slip D.J., Shine R. Reptilian endothermy: a field study of thermoregulation by brooding diamond pythons // J. Zool. 1988. V. 216 (2). P. 367–378.

  155. Smith E.N. Thermoregulation of the American alligator, Alligator mississippiensis // Physiol. Zool. 1975. V. 48 (2). P. 177–194.

  156. Smith E., Morowitz H.J. Universality in intermediary metabolism // PNAS USA. 2004. V. 101. P. 13168–13173.

  157. Smith W.S., Broadbridge R., East J.M., Lee A.G. Sarcolipin uncouples hydrolysis of ATP from accumulation of Ca2+ by the Ca2+-ATPase of skeletal-muscle sarcoplasmic reticulum // Biochem. J. 2002. V. 361. P. 277–286.

  158. Snow R.W., Wolf A.J., Greeves B.W. et al. Thermoregulation by a brooding Burmese python (Python molurus bivittatus) in Florida // Southeast. Nat. 2010. V. 9. P. 403–405.

  159. Stager M., Cheviron Z.A. Is there a role for sarcolipin in avian facultative thermogenesis in extreme cold? // Biol. Lett. 2020. V. 16. P. 20200078.

  160. Stahlschmidt Z.R., Denardo D.F. Effect of nest temperature on egg-brooding dynamics in Children’s pythons // Physiol. Behav. 2009. V. 98. P. 302–306.

  161. Standora E.A., Spotila J.R., Foley R.E. Regional endothermy in the sea turtle, Chelonia mydas // J. Therm. Biol. 1982. V. 7. P. 159–165.

  162. Stevens E.D. The retia // Encyclopedia of fish physiology: from genome to environment / Ed. A.P. Farrell. San Diego: Acad. Press, 2011. P. 1119–1131.

  163. Swanson D. Seasonal metabolic variation in birds: functional and mechanistic correlates // Current ornithology. V. 17 / Ed. C.F. Thompson. N.Y.: Springer, 2010. P. 75–129.

  164. Talbot D.A., Duchamp C., Rey B. et al. Uncoupling protein and ATP/ADP carrier increase mitochondrial proton conductance after cold adaptation of king penguins // J. Physiol. 2004. V. 558. P. 123–135.

  165. Tattersall G.J. Reptile thermogenesis and the origins of endothermy // Zoology. 2016. V. 119. P. 403–405.

  166. Tattersall G.J., Milsom W.K., Abe A.S. et al. The thermogenesis of digestion in rattlesnakes // J. Exp. Biol. 2004. V. 207. P. 579–585.

  167. Tattersall G.J., Leite C.A., Sanders C.E. et al. Seasonal reproductive endothermy in tegu lizards // Adv. 2016. V. 2. P. e1500951

  168. Teulier L., Rouanet J.L., Letexier D. et al. Cold-acclimation-induced nonshivering thermogenesis in birds is associated with upregulation of avian UCP but not with innate uncoupling or altered ATP efficiency // J. Exp. Biol. 2010. V. 213. P. 2476–2482.

  169. Teulier L., Rouanet J.L., Rey B., Roussel D. Ontogeny of nonshivering thermogenesis in muscovy ducklings (Cairina moschata) // Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2014. V. 175. P. 82–89.

  170. Tigerstedt R. Die Produktion von Wärme und der Wärmehaushalt. Handbuch der vergleichenden Physiologie / Herausg. von H. Winterstein. Jéna: Springer, 1910. 1060 S.

  171. Torre-Bueno J.R., Larochelle J. The metabolic cost of flight in unrestrained birds // J. Exp. Biol. 1978. V. 75. P. 223–229.

  172. Toyomizu M., Ueda M., Sato S. et al. Cold-induced mitochondrial uncoupling and expression of chicken UCP and ANT mRNA in chicken skeletal muscle // FEBS Lett. 2002. V. 529. P. 313–318.

  173. Tucker V.A. Respiratory exchange and evaporative water loss in the flying budgerigar // J. Exp. Biol. 1968. V. 48. P. 67–87.

  174. Tucker V.A. Metabolism during flight in the laughing gull, Larus atricilla // Am. J. Physiol. 1972. V. 222. P. 237–245.

  175. Ueda M., Watanabe K., Sato K. et al. Possible role for avPGC‑1alpha in the control of expression of fiber type, along with avUCP and avANT mRNAs in the skeletal muscles of cold-exposed chickens // FEBS Lett. 2005. V. 579. P. 11–17.

  176. Valensiennes A. Obsrevations faites pendant l’incubation d’une femelle du python a deux raies (Python bivittatus, Kuhl.) pendant les mois de mai et de juin 1841. Paris: Comp. Rend. Acad. Sci., 1841. V. 13. P. 126–133.

  177. van Mierop L.H.S., Barnard S.M. Observations on the reproduction of Python molurus bivittatus (Reptilia, Serpentes, Boidae) // J. Herpetol. 1976a. V. 10 (4). P. 333–340.

  178. van Mierop L.H.S., Barnard S.M. Thermoregulation in a brooding female Python molurus bivittatus (Serpentes: Boidae) // Copeia. 1976b. № 2. P. 398–401.

  179. Vernon H.M. The relation of the respiratory exchange of cold-blooded animals to temperature // J. Phisiol. 1897. V. 21. P. 443–496.

  180. Walter I., Seebacher F. Endothermy in birds: underlying molecular mechanisms // J. Exp. Biol. 2009. V. 212. P. 2328–2336.

  181. Wang W.P., Wang J.Y., Lin W.H. et al. Progerin in muscle leads to thermogenic and metabolic defects via impaired calcium homeostasis // Aging Cell. 2020. V. 19. P. e13090.

  182. Ward S., Moller U., Rayner J.M. et al. Metabolic power, mechanical power and efficiency during wind tunnel flight by the European starling Sturnus vulgaris // J. Exp. Biol. 2001. V. 204. P. 3311–3322.

  183. Watanabe Y., Goldman K., Caselle J. et al. Comparative analyses of animal-tracking data reveal ecological significance of endothermy in fishes // PNAS USA. 2015. V. 112. P. 6104–6109.

  184. Wegner N.C., Snodgrass O.E., Dewar H., Hyde J.R. Animal physiology. Whole-body endothermy in a mesopelagic fish, the opah, Lampris guttatus // Science. 2015. V. 348. P. 786–789.

  185. Whitney M.R., Otoo B.K.A., Angielczyk K.D., Pierce S.E. Fossil bone histology reveals ancient origins for rapid juvenile growth in tetrapods // Commun. Biol. 2022. V. 5. P. 1280.

  186. Ye J.M., Edwards S.J., Rose R.W. et al. Vasoconstrictors alter oxygen, lactate, and glycerol metabolism in the perfused hindlimb of a rat kangaroo // Am. J. Physiol. 1995. V. 268. P. R1217–R1223.

  187. Ye J.M., Edwards S.J., Rose R.W. et al. Alpha-adrenergic stimulation of thermogenesis in a rat kangaroo (Marsupialia, Bettongia gaimardi) // Am. J. Physiol. 1996. V. 271. P. R586–R582.

  188. Zhang Y., Carter T., Eyster K., Swanson D.L. Acute cold and exercise training up-regulate similar aspects of fatty acid transport and catabolism in house sparrows (Passer domesticus) // J. Exp. Biol. 2015. V. 218. P. 3885–3893.

Дополнительные материалы отсутствуют.