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Endothermy in fishes: a phylogenetic analysis of constraints, predispositions, and selection pressures

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Endothermy, the ability to raise body temperature by internal heat production, is unusual in teleost fishes and has only been documented within one suborder, the Scombroidei. Two separate modes of endothermy have evolved in the scombroidei; tunas warm their muscles, brain and viscera using heat exchangers in the circulation to these metabolically active tissues while billfishes and one primitive mackerel have a thermogenic organ situated beneath the brain. Both modes of endothermy emphasize common themes. Large body size coupled with heat exchangers are necessary to reduce convective and conductive heat exchange. A tissue with a high oxidative capacity is required for heat generation. Studies based upon morphology and mitochondrial DNA analyses indicate that endothermy has evolved independently at least three times within the scombroid lineage. Mapping of-morphological and physiological traits on a molecular phylogeny for scombroids provides evidence of selective pressures favoring evolution of diverse endothermic styles. The new results suggest anatomical constraints prevent most fish from using the tuna form of endothermy and indicate a possible linkage between endothermy and locomotory style (thunniform or sub-carangiform).

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References cited

  • Alexander, R.M. 1969. The orientation of muscle fibres in the myotomes of fishes. J. Mar. Biol. Assoc. U.K. 49: 263–290.

    Google Scholar 

  • Bach-y-Rita, R. & F. Ito. 1966. In vivo studies of fast and slow muscle fibers in cat extraocular muscle. J. Gen. Physiol. 49: 1177–1198.

    PubMed  Google Scholar 

  • Baker, M.A. 1982. Brain cooling in endotherms in heat and exercise. Annual. Rev. Physiol. 44: 85–96.

    PubMed  Google Scholar 

  • Ballantyne, J.S., M.E. Chamberlin & T.D. Singer. 1992. Oxidative metabolism in thermogenic tissues of swordfish and mako shark. J. Exp. Zool. 261: 110–114.

    Google Scholar 

  • Bennett, A.F. & J.A. Ruben. 1979. Endothermy and activity in vertebrates. Science 206: 649–653.

    PubMed  Google Scholar 

  • Block, B.A. 1986. Structure of the brain and eye heater tissue in marlins, sailfish, and spearfishes. J. Morph. 190: 169–189.

    PubMed  Google Scholar 

  • Block, B.A. 1987. Billfish brain and eye heater: a new look at nonshivering heat production. News in Physiological Sciences 2: 208–213.

    Google Scholar 

  • Block, B.A. 1990. Phylogeny and ecology of brain and eye heaters in billfishes. pp. 123–136.In: R.H. Stroud (ed.) Planning the Future of Billfishes, National Coalition for Marine Conservation, Savannah.

    Google Scholar 

  • Block, B.A. 1991. Endothermy in fish: thermogenesis, ecology and evolution. pp. 269–311.In: P.W. Hochachka & T. Mommsen (ed.) Biochemistry and Molecular Biology of Fishes, Vol 1, Elsevier, New York.

    Google Scholar 

  • Block, B.A. 1994. Thermogenesis in muscle. Annual Reviews of Physiology. 56: 535–577.

    Google Scholar 

  • Block, B.A. & F.G. Carey. 1985. Warm brain and eye temperatures in sharks. J. Comp. Physiol. B. 156: 229–236.

    PubMed  Google Scholar 

  • Block, B.A. & C. Franzini-Armstrong. 1988. The structure of the membrane systems in a novel muscle cell modified for heat production. J. Cell Biol. 107: 1099–1112.

    PubMed  Google Scholar 

  • Block, B.A., J.D. Finnerty, A.F.R. Stewart & J. Kidd. 1993. Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny. Science 260: 210–214.

    PubMed  Google Scholar 

  • Bone, Q. 1966. On the function of the two types of myotomal muscle fibres in elasmobranch fish. J. Mar. Biol. Assoc. U.K. 46: 321–349.

    Google Scholar 

  • Bone, Q. 1971. On the scabbard fish,Aphanopus carbo. J. Mar. Biol. Assoc. U.K. 51: 219–225.

    Google Scholar 

  • Bone, Q. & A.D. Chubb. 1983. The retial system of the locomotor muscles in the thresher shark. J. Mar. Biol. Assoc. U.K. 63: 239–241.

    Google Scholar 

  • Brooks, D.R. & D.A. Maclennan. 1991. Phylogeny, ecology, and behavior. A research program in comparative biology. University of Chicago Press, Chicago. 434 pp.

    Google Scholar 

  • Brill, R.W., D.L. Guernsey & E.D. Stevens. 1978. Body surface and gill heat loss rates in restrained skipjack tuna. pp. 261–276.In: G.D. Sharp & A.E. Dizon (ed.) The Physiological Ecology of Tunas, Academic Press, New York.

    Google Scholar 

  • Brill, R.W, H. Dewar & J.B. Graham. 1994. Basic concepts relevant and gill heat loss rates in restrained skipjack tuna. to heat transfer in fishes, and their use in measuring the physiological thermoregulatory abilities of tunas. Env. Biol. Fish. (in press).

  • Bushnell, P.G., D.R. Jones & A.P. Farrell. 1992. The arterial system. pp. 89–139.In: W.S. Hoar, D.J. Randall & A.P. Farrell (ed) Fish Physiology, Vol 12, Academic Press, San Diego.

    Google Scholar 

  • Carey, F.G. 1982a. Warm fish. pp. 216–233.In: C.R. Taylor, K. Kohansen & L. Bolis (ed.) A Companion to Animal Physiology, Cambridge University Press, Cambridge.

    Google Scholar 

  • Carey, F.G. 1982b. A brain heater in the swordfish. Science 216: 1327–1329.

    PubMed  Google Scholar 

  • Carey, F.G. 1990. Further observations on the biology of the swordfish. pp. 103–122.In: R.H. Stroud (ed.) Planning the Future of Billfishes, National Coalition for Marine Conservation, Savannah.

    Google Scholar 

  • Carey, F.G. & J.M. Teal. 1966. Heat conservation in tuna fish muscle. Proc. Natl. Acad. Sci. U.S.A. 56: 1464–1469.

    Google Scholar 

  • Carey, F.G., J.M. Teal, J.W. Kanwisher & K.D. Lawson. 1971. Warm-bodied fish. Amer. Zool. 11: 137–145.

    Google Scholar 

  • Carey, F.G., J.M. Teal & J.W. Kanwisher. 1981. The visceral temperatures of mackerel sharks. Physiol. Zool. 54: 334–344.

    Google Scholar 

  • Carey, F.G., J.G. Casey, H.L. Pratt, D. Urkuhart & J.E. McCosker. 1985. Temperature, heat production and heat exchange in lamnid sharks. Memoirs of the Southern California Academy of Science 9: 92–108.

    Google Scholar 

  • Carey, F.G. & Q. Gibson. 1987. Blood flow in the muscle of free-swimming fish. Physiol. Zool. 60: 138–148.

    Google Scholar 

  • Carey, F.G. & J.V. Scharold. 1990. Movements of blue sharks in course and depth. Mar. Biol. 106: 329–342.

    Google Scholar 

  • 1978. Adaptations and systematics of the mackerels and tunas. pp. 7–40.In: G.D. Sharp & A.E. Dizon (ed.) The Physiological Ecology of Tunas, Academic Press, New York.

    Google Scholar 

  • Collette, B.B., T. Potthoff, W.J. Richards, S. Ueyanagi, J.L. Russo & Y. Nishikawa. 1984. Scombroidei: development and relationships. pp. 591–620.In: H.G. Moser et al. (ed.) Ontogeny and Systematics of Fishes, Special Publication No. 1, American Society of Ichthyologists and Herpetologists, Lawrence

    Google Scholar 

  • Compagno, L.G.V. 1984. Sharks of the world. FAO Fisheries Synopsis No. 125, 4: 1–655.

    Google Scholar 

  • Crompton, A.W, C.R. Taylor & J.A. Jagger. 1978. Evolution of homeothermy in mammals. Nature 272: 333–336.

    PubMed  Google Scholar 

  • Dean, J.M. 1976. Temperature of tissues in freshwater fishes. Trans. Amer. Fish. Soc. 6: 709–711.

    Google Scholar 

  • Denton, R.M. & J.G. McCormack. 1990. Ca2+ as a second messenger within mitochondria of the heart and other tissues. Ann. Rev. Physiol. 52: 451–466.

    Google Scholar 

  • Dickson, K.A. 1988. Why are some fishes endothermic? Inter-specific comparisons of aerobic and anerobic metabolic capacities in endothermic and ectothermic scombrids. Ph.D. Dissertation, University of California, San Diego. 358 pp.

    Google Scholar 

  • Dickson, K.A., A.V. Dall, J.M. Eisman, E.T. McDonnell & A.M. Hendrzak. 1988. Biochemical indices of aerobic and anaerobic capacity in red and white myotomal muscle of active, pelagic sharks: comparisons between endothermic and ectothermic species. Journal of the Pennsylvania Academy of Science 62 (3): 147–151.

    Google Scholar 

  • Dickson, K.A. 1994. Unique adaptations of the metabolic biochemistry of tunas and billfishes for life in the pelagic environment. Env. Biol. Fish. (in press).

  • Finnerty, J.R. & B.A. Block. Evolution of cytochrome b in Scombroidei (Teleostei); insights into billfish relationships. U.S. Fish. Bull. (in press).

  • Gibbs, R.H. & B.B. Collette. 1967. Comparative anatomy and systematics of the tunas, genusThunnus. U.S. Fish Bull. 66: 65–130.

    Google Scholar 

  • Graham, J.B. 1975. Heat exchange in the yellowfin tuna,Thunnus albacares, and skipjack tuna,Katsuwonus pelamis, and the adaptive significance of elevated body temperatures in scombrid fishes. U.S. Fish. Bull. 73: 219–229.

    Google Scholar 

  • Graham, J.B. 1983. Heat transfer. pp. 248–279.In: P.W. Webb & D. Weihs (ed.) Fish Biomechanics, Praeger Publishers, New York.

    Google Scholar 

  • Graham, J.B., F.J. Koehrn & K.A. Dickson. 1983. Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to locomotion and endothermy. Can. J. Zool. 61: 2087–2096.

    Google Scholar 

  • Guppy, M., W.C. Hulbert & P.W. Hochachka. 1979. Metabolic sources of heat and power in tuna muscles. II. Enzyme and metabolite profiles. J. Exp. Biol. 82: 303–320.

    PubMed  Google Scholar 

  • Hebrank, J.H., M.R. Hebrank, J.H. Long, B.A. Block & S.A. Wainwright. 1990. Backbone mechanics of the blue marlinMakaira nigricans (Pisces, Istiophoridae). J. Exp. Biol. 148: 449–459.

    Google Scholar 

  • Himms-Hagen, J. 1991. Brown adipose tissue thermogenesis: interdisciplinary studies. FASEB J. 4: 2890–2898.

    Google Scholar 

  • Hochachaka, P.W. & R.W. Brill. 1987. Autocatalytic pathways to cell death: a new analysis of the tuna burn problem. Fish Physiol. Biochem. 4: 81–87.

    Google Scholar 

  • Holland, K.N., R.W. Brill, R.K.C. Chang, J.R. Sibert & D.A. Fournier. 1992. Physiological and behavioral thermoregulation in bigeye tune (Thunnus obesus) Nature 358: 410–412.

    PubMed  Google Scholar 

  • Huey, R.B. 1987. Phylogeny, history, and the comparative method. pp. 76–98.In: M.E. Feder, A.F. Bennett, W.W. Burggren & R.B. Huey (ed.) New Directions in Physiological Ecology, Cambridge University Press, Cambridge

    Google Scholar 

  • Hulbert, W.C., M. Guppy, B. Murphy & P.W. Hochachka. 1979. Metabolic sources of heat and power in tuna muscles. I. Muscle fine structure. J. Exp. Biol. 82: 289–301.

    PubMed  Google Scholar 

  • Johnson, G.D. 1986. Scombroid phylogeny: an alternative hypothesis. Bull. Mar. Sci. 39: 1–41.

    Google Scholar 

  • Lindsey, C.C. 1978. Form, function, and locomotory habits in fish. pp. 1–100.In: W.S. Hoar & D.J. Randall (ed.) Fish Physiology, Vol. 7, Academic Press, New York.

    Google Scholar 

  • Linthicum, D.S. & F.G. Carey. 1971. Regulation of brain and eye temperatures by the bluefin tuna. Comp. Biochem. Physiol. 43A: 425–433.

    Google Scholar 

  • Maddison, W.P. & D.R. Maddison. 1992. MacClade: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland. 398 pp.

    Google Scholar 

  • Martin, A.P, G.J.P. Naylor & S.R. Palumbi. 1992. Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357: 153–155.

    PubMed  Google Scholar 

  • MacClennan, D.H. & M.S. Phillips. 1992. Malignant hyperthermia. Science 256: 789–794.

    PubMed  Google Scholar 

  • Moyes, C.D., O.A. Mathieu-Costello, R.W. Brill & P.W. Hochachka. 1992. Can. J. Zool. 70: 1246–1253.

    Google Scholar 

  • Neill, W.H. & E.D. Stevens. 1974. Thermal inertia versus thermoregulation in ‘warm’ turtles and tunas. Science 184: 1008–1010.

    PubMed  Google Scholar 

  • Neill, W.H., R.K. Chang & A.E. Dizon. 1976. Magnitude and ecological importance of thermal inertia in skipjack tuna,Katsuwonnus pelamis (Linneaus). Env. Biol. Fish. 1: 61–80.

    Google Scholar 

  • O'Brien, J., A. Tullis & B.A. Block. 1992. Role of mitochondria in heat production by a muscle derived thermogenic organ in fish. Biophys. J. 61: A297.

    Google Scholar 

  • O'Brien, J., G. Meissner & B.A. Block. 1994. The fastest contracting muscles of non-mammalian vertebrates express only one isoform of the ryanodine receptor. Biophysical J. 65: 2418–2427.

    Google Scholar 

  • Prosser, C.L. & C.O. Nelson. 1981. The role of nervous systems in temperature adaptation of poikilotherms. Ann. Rev. Physiol. 43: 281–300.

    Google Scholar 

  • Rayner, M.D. & M.J. Keenan. 1967. Role of red and white muscles in the swimming of skipjack tuna. Nature 214: 392–393.

    PubMed  Google Scholar 

  • Ridley, M. 1983. The explanation of organic diversity: the comparative method and adaptations for mating. Clarendon Press, Oxford. 272 pp.

    Google Scholar 

  • Rome, L.C., R.P. Funke, R.M. Alexander, G. Lutz, H.D.J.N. Aldridge, F. Scott & M. Freadman. 1988. Why animals have different muscle fiber types. Nature 355: 824–827.

    Google Scholar 

  • Sharp, G.D. & S.W. Pirages. 1978. The distribution of red and white swimming muscle, their biochemistry and the biochemistry phylogeny of selected scombrid fishes. pp. 41–78.In: G. Sharp & A. Dizon (ed.) The Physiological Ecology of Tunas, Academic Press, New York.

    Google Scholar 

  • Sidell, B.D. & T.S. Moerland. 1989. Effects of temperature on muscular function and locomotory performance in teleost fish. pp. 115–156.In: C. Magnum (ed.) Advances in Comparative and Environmental Physiology, Vol. 5, Springer-Verlag, Berlin.

    Google Scholar 

  • Sidell, B.D., W.R. Driedzic, D.B. Stowe & I.A. Johnston. 1987. Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiol. Zool. 60: 221–232.

    Google Scholar 

  • Stevens, E.D. & F.E. Fry. 1971. Brain and muscle temperatures in ocean caught and captive skipjack tuna. Comp. Biochem. Physiol. 1971: 203–211.

    Google Scholar 

  • Stevens, E.D. & F. G. Carey. 1981. One why of the warmth of warm-bodied fish. Amer. J. Physiol. 240: R151–R155.

    Google Scholar 

  • Suarez, R.K., M.D. Mallet, C. Daxboeck & P.W. Hochachka. 1986. Enzymes of energy metabolism and gluconeogenesis in the Pacific blue marlin,Makaira nigricans. Can. J. Zool. 64: 694–697.

    Google Scholar 

  • Tullis, A., B.A. Block & B.D. Sidell. 1991. Activities of key metabolic enzymes in the heater organs of scombroid fishes. J. Exp. Biol. 161: 383–403.

    PubMed  Google Scholar 

  • Tullis, A. & B.a. Block. 1992. On the origin of the billfish heater cell phenotype. Amer. Zool. 32: 68A.

    Google Scholar 

  • Watson, C., R.E. Bourke & R.W. Brill. 1988. A comprehensive theory on the etiology of burnt tuna. U.S. Fish. Bull. 86: 372–376.

    Google Scholar 

  • Westneat, M.W. W. Hoese, C.A. Pell & S.A. Wainwright. 1993. Locomotor mechanisms of force transfer in the horizontal septum of scombrid fishes. J. Morphol. 217: 183–204.

    Google Scholar 

  • White, F.C., R. Kelly, S. Demper, P.T. Schumacker, K.R. Gallagher & R.M. Laurs. 1988. Organ blood flow hemnodynamics and metabolism of the albacore tunaThunnus alalunga (Bonnaterre). Exp. Biol. 47: 161–169.

    PubMed  Google Scholar 

  • Wolf, N.G., P.R. Swift & F.G. Carey. 1988. Swimming muscle helps warm the brain of lamnid sharks. J. Comp. Physiol. B. 157: 709–715.

    Google Scholar 

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  1. Barbara A. Block

    Present address: Hopkins Marine Station, Stanford University, 93950, Pacific Grove, CA, USA

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  1. Department of Organismal Biology and Anatomy, The University of Chicago, 1027 East 57th Street, Chicago, IL, 60637, USA

    Barbara A. Block & John R. Finnerty

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Paper from the International Union of Biological Societies symposium ‘The biology of tunas and billfishes: an examination of life on the knife edge’, organized by Richard W. Brill and Kim N. Holland.

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Block, B.A., Finnerty, J.R. Endothermy in fishes: a phylogenetic analysis of constraints, predispositions, and selection pressures. Environ Biol Fish 40, 283–302 (1994). https://doi.org/10.1007/BF00002518

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