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Did lungs and the intracardiac shunt evolve to oxygenate the heart in vertebrates?

  • Colleen Farmer (a1)
Abstract

Traditional wisdom of the evolution of lungs in fishes is that lungs arose when gill ventilation was hindered by an aquatic habitat that was low in oxygen. This scenario has been buttressed primarily by a proposed correlation between extant air-breathing fishes and hypoxic habitats, as well as by the fact that early vertebrate fossils were found in sediments believed to indicate a semi-arid environment. There are problems with this scenario, yet it retains a dominant influence on how the evolution of aerial respiration is viewed. This paper presents a new hypothesis for lung evolution that is more consistent with the fossil record and physiology of extant animals than the traditional scenario; I propose that lungs evolved to supply the heart with oxygen. The primitive vertebrate heart was spongy in architecture and devoid of coronary support, obtaining oxygen from luminal blood. By supplying oxygen to this tissue, lungs may have been important in ancient fishes for sustaining activity, regardless of environment. Furthermore, this function for lungs may have influenced cardiovascular adaptations of tetrapods because their divided cardiovascular system isolates the right side of the heart from pulmonary oxygen. I propose that three innovations compensate for this isolation: In extant amphibians oxygen-rich blood from cutaneous and buccal respiration enters the right side of the heart; in chelonians and lepidosaurs the intracardiac shunt washes oxygen-rich blood into the right side of the heart; in mammals, birds, and perhaps in crocodilians, support of the heart by coronary vasculature eliminates this problem.

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Barrell J. 1916. Influence of Silurian–Devonian climates on the rise of airbreathing vertebrates. Geological Society of America Bulletin 27:387436.
Bates D. W., and Vinsonhaler R. 1957. The use of louvers as a means of guiding fish at the Tracy, California, pumping plant. Transactions of the American Fisheries Society for 1956 86:3857.
Beamish F. W. H. 1966. Muscular fatigue and mortality in haddock, Melanogrammus aeglefinus, caught by otter trawl. Journal of the Fisheries Resource Board of Canada 23:15071521.
Becker G. C. 1983. Fishes of Wisconsin. University of Wisconsin, Madison.
Bennett A. F. 1978. Activity metabolism of the lower vertebrates. Annual Review of Physiology 400:447469.
Black E. C. 1955. Blood levels of hemoglobin and lactic acid in some freshwater fishes following exercise. Journal of the Fisheries Resource Board of Canada 12:917929.
Black E. C. 1957a. Alterations in the blood level of lactic acid in certain salmonoid fishes following muscular activity. I. Kamloops trout, Salmo gairdneri. Journal of the Fisheries Resource Board of Canada 14:117134.
Black E. C. 1957b. Alterations in the blood level of lactic acid in certain salmonoid fishes following muscular activity. II. Lake trout, Salvelinus namaycush. Journal of the Fisheries Resource Board of Canada 14:645649.
Black E. C. 1957c. Alterations in the blood level of lactic acid in certain salmonoid fishes following muscular activity. III. Sockeye salmon, Oncorhynchus nerka. Journal of the Fisheries Resource Board of Canada 14:807814.
Black E. C. 1958. Hyperactivity as a lethal factor in fish. Journal of the Fisheries Resource Board of Canada 15:573586.
Black E. C., Robertson Connor A., Lam K., and Chiu W. 1962. Changes in glycogen, pyruvate and lactate in rainbow trout (Salmo gairdneri) during and following muscular activity. Journal of the Fisheries Resource Board of Canada 19:409436.
Boucot A., and Janis C. 1983. Environment of the early Paleozoic vertebrates. Palaeogeography, Palaeoclimatology, Palaeoecology 41:251287.
Brady A. J., and Dubkin C. 1964. Coronary circulation in the turtle ventricle. Biochemical Physiology 13:119128.
Brainerd E. L. 1994. The evolution of lung-gill bimodal breathing and the homology of vertebrate respiratory pumps. American Zoologists 34:289299.
Bray A. A. 1985. The evolution of the terrestrial vertebrates: environmental and physiological considerations. Philosophical Transactions of the Royal Society of London B 309:289322.
Breisch E. A., White F., Jones H. M., and Laurs R. M. 1983. Ultrastructural morphometry of the myocardium of Thunnus alalunga. Cell and Tissue Research 233:427438.
Burggren W., and Randall D. 1978. Oxygen uptake and transport during hypoxic exposure in the sturgeon Acipenser transmontanus. Respiration Physiology 34:171183.
Coates M. I., and Clack J. A. 1995. Romer's gap: tetrapod origins and terrestriality. Bulletin du Museum national d'Histoire naturelle 4e séries 17:373388.
Daeschler E. B., and Shubin N. H. 1995. Tetrapod origins. Paleobiology 21:404409.
Davie P. S., and Farrell A. P. 1991. The coronary and luminal circulations of the myocardium of fishes. Canadian Journal of Zoology 69:19932001.
Denison R. H. 1951. Late Devonian fresh-water fishes from the western United States. Fieldiana (Geology) 11:221261.
Denison R. H. 1956. A review of the habitat of the earliest vertebrates. Fieldiana (Geology) 11:361457.
Denison R. H. 1968. Early Devonian lungfishes from Wyoming, Utah and Idaho. Fieldiana (Geology) 17:353413.
Driedzic W. R., and Gesser H. 1994. Energy metabolism and contractility in ectothermic vertebrate hearts: hypoxia, acidosis, and low temperature. Physiological Reviews 74:221258.
Emery S. H., Mangano C., and Randazzo V. 1985. Ventricle morphology in pelagic elasmobranch fishes. Comparative Biochemistry and Physiology A82: 635–543.
Farmer C. G., and Jackson D. C. 1995. The importance of lung ventilation during activity in Amia calva. American Zoologist 35:62A.
Farrell A. P. 1984. A review of cardiac performance in the teleost heart: intrinsic and humoral regulation. Canadian Journal of Zoology 62:523536.
Farrell A. P., and Jones D. R. 1992. The heart. In Hoar W. S., Randall D. J., and Farrell A. P., eds. Fish Physiology 12(A):188Academic Press, San Diego.
Farrell A. P., Small S., and Graham M. S. 1989. Effect of heart rate and hypoxia on the performance of a perfused trout heart. Canadian Journal of Zoology 67:274280.
Foxon G. E. H. 1950. A description of the coronary arteries in dipnoan fishes and some remarks on their importance from the evolutionary standpoint. Journal of Anatomy, London 84:121131.
Foxon G. E. H. 1955. Problems of the double circulation in vertebrates. Biological Reviews 30:196228.
Fricke H., Hissmann K., Schauer J., Reinicke O., Kasang L., and Plante R. 1991. Habitat and population size of the coelacanth Latimeria chalumnae at Grand Comoro. Environmental Biology of Fishes 32:287300.
Gans C. 1970. Respiration in early tetrapods—the frog is a red herring. Evolution 24:723734.
Gans C. 1989. Stages in the origin of vertebrates: analysis by means of scenarios. Biological Reviews 64:221268.
Gesser H. 1985. Effects of hypoxia and acidosis on fish heart performance. Pp. 402410In Gilles R., ed. Respiration and metabolism: current comparative approaches. Springer, Berlin.
Gesser H., and Poupa O. 1983. Acidosis and cardiac muscle contractility: comparative aspects. Comparative Biochemistry and Physiology 76A:559566.
Gesser H., Andresen P., Brams P., and Sund-Laursen J. 1982. Inotropic effects of adrenaline on the anoxic or hypercapnic myocardium of rainbow trout and eel. Journal of Comparative Physiology 147:123128.
Goodyear P. C. 1967. Feeding habits of three species of gars, Lepisosteus, along the Mississippi gulf coast. Transactions of the American Fisheries Society 96:297300.
Graham J. B. 1976. Respiratory adaptations of marine air-breathing fishes. Pp. 165187In Hughes G. M., ed. Respiration of amphibious vertebrates. Academic Press, London.
Graham J. B. 1994. An evolutionary perspective for bimodal respiration: a biological synthesis of fish air breathing. American Zoologist 34:229237.
Graham M. S., and Farrell A. P. 1990. Myocardial oxygen consumption in trout acclimated to 5° and 15°C. Physiological Zoology 63:536554.
Grant R. T., and Regnier M. 1926. The comparative anatomy of the cardiac coronary vessels. Heart 13:285317.
Grigg G. 1965. Studies on the Queensland lungfish, Neoceratodus Forsteri (Krefft) III. Aerial respiration in relation to habits. Australian Journal of Zoology 13:413421.
Gunther A. 1871a. Description of Ceratodus, a genus of Ganoid fishes, recently discovered in rivers of Queensland, Australia. Philosophical Transactions of the Royal Society of London 161:511571.
Gunther A. 1871b. The new Ganoid fish from Queensland (Ceratodus). Nature 1871:406408.
Hicks J. W. 1993. Mechanism of intracardiac shunting in reptiles. Pp. 249259In Scheid P., ed. Respiration in health and disease. G. Fischer Verlag, Stuttgart.
Hicks J. W. 1994. Adrenergic and cholinergic regulation of intracardiac shunting. Physiological Zoology 67:13251346.
Hicks J. W. 1995. Cardiac shunting in reptiles: mechanisms, regulation and physiological function. In Gans C. and Gaunt A. S., eds. The biology of the Reptilia. Morphology, Vol. G, The visceral organs. Society for the Study of Amphibians and Reptiles, Ithaca, N.Y.
Hicks J. W., and Wood S. C. 1989. Oxygen homeostasis in lower vertebrates: the impact of external and internal hypoxia. Pp. 311341In Wood S. C., ed. Comparative pulmonary physiology. Marcel Dekker, New York.
Hochachka P. W., Guppy M., Guderley H., Storey K. B., and Hulbert W. C. 1978. Metabolic biochemistry of water- vs. air-breathing in osteoglossids: heart enzymes and ultrastructure. Canadian Journal of Zoology 56:759768.
Jackson D. C., Shi H., Singer J. H., Hamm P. H., and Lawler R. G. 1995. Effects of input pressure on in vitro turtle heart during anoxia and acidosis: a 31P-NMR study. American Journal of Physiology 268 (Regulatory Integrative Comparative Physiology 37):R683R689.
Johansen K. 1970. Air breathing in fishes. Pp. 361411In Hoar W. S. and Randall D. J., eds. Fish physiology, Vol. 4. Academic Press, New York.
Johansen K. 1985. A Phylogenetic overview of cardiovascular shunts. Pp. 1732In Johansen K. and Burggren W., eds. Alfred Benzon Symposium 21: Cardiovascular shunts; phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen.
Johansen K., and Burggren W. 1980. Cardiovascular function in the lower vertebrates. Pp. 61117In Bourne G. H., ed. Hearts and heart-like organs. Academic Press, New York.
Johansen K., and Hanson D. 1968. Functional anatomy of the hearts of lungfishes and amphibians. American Zoologist 8:191210.
Johansen K., and Lenfant C. 1967. Respiratory function in the South American lungfish, Lepidosiren paradoxa (Fitz). Journal of Experimental Biology 46: 205–18.
Johansen K., Lenfant C., and Grigg G. C. 1967. Respiratory control in the lungfish, Neoceratodus forsteri (Krefft). Comparative Biochemistry and Physiology 20:835845.
Johansen K., Lenfant C., and Hanson D. 1968. Cardiovascular dynamics in the lungfishes. Zeitschrift für vergleichende Physiologie 59:157186.
Johansen K., Hanson D., and Lenfant C. 1970. Respiration in a primitive air breather, Amia calva. Respiration Physiology 9:162174.
Jones D. R., and Randall D. J. 1978. The respiratory and circulatory systems during exercise. In Hoar W. S. and Randall D. J., eds. Fish Physiology 7:425501. Academic Press, New York.
Kiceniuk J. W., and Jones D. R. 1977. The oxygen transport system in trout (Salmo gairdneri) during sustained exercise. Journal of Experimental Biology 69:247260.
Kohmoto T., Argenziano M., Yamamoto N., Vliet K. A., Gu A., DeRosa C. M., Fisher P., Spotnitz H. M., Burkhoff D., and Smith C. R. 1997. Assessment of transmyocardial perfusion in alligator hearts. Circulation 95:15851591.
Kramer D. L., Lindsey C. C., Moodie G. E. E., and Stevens E. D. 1978. The fishes and the aquatic environment of the central Amazon basin, with particular reference to respiratory patterns. Canadian Journal of Zoology 56:717729.
Krefft G. 1870. Description of a gigantic amphibian allied to genus Lepidosiren, from Wide Bay district, Queensland. Proceedings of the Zoological Society of London 1870:221224.
Krosniunas E. H., and Hicks J. W. 1994. Cardiovascular correlates of behavior in the turtle. The Physiologist 37(5):A-95[Abstract.]
Lenfant C., and Johansen K. 1968. Respiration in the African lungfish Protopterus aethiopicus: I. Respiratory properties of blood and normal patterns of breathing and gas exchange. Journal of Experimental Biology 49:437452.
Liem K. F. 1988. Form and function of lungs: The evolution of air breathing mechanisms. American Zoologist 28:739759.
MacKinnon M. R., and Heatwole H. 1981. Comparative cardiac anatomy of the reptilia. IV. The coronary arterial circulation. Journal of Morphology 170:127.
Magid A. M. A. 1966. Breathing and function in the spiracles in Polypterus senegalus. Animal Behavior 14:530533.
Maisey J. G. 1996. Discovering fossil fishes. H. Holt, New York.
Mallatt J. 1985. Reconstructing the life cycle and the feeding of ancestral vertebrates. Pp. 5968In Foreman R. E., Gorbman A., Dodd J. M., and Olsson R., eds. Evolutionary biology of primitive fishes. Plenum, New York.
Martin D., Grably S., Royer F., Benchetrit G., Rossi A., Tota B., Marciano V., Farina F. and Zummo G. 1987. Metabolic alterations induced by hypoxia in the tortoise heart, comparison between spongy and compact myocardium. Comparative Biochemistry and Physiology 86A:319323.
Matthew W. D. 1915. Climate and evolution. Annals of the New York Academy of Sciences 24:171318.
Millot J., Anthony J. and Robineau J. 1978. Anatomie de Latimeria chalumnae, Vol. 3. Centre nationale de la Recherche scientifique, Paris.
Morris C. 1892. The origin of lungs, a chapter in evolution. American Naturalist 26:975986.
Navaratnam V. 1980. Anatomy of the mammalian heart. Pp. 349374In Bourne G. H., ed. Hearts and heart-like organs. Academic Press, New York.
Nelson J. S. 1984. Fishes of the world. Wiley, New York.
Packard G. C. 1974. The evolution of air-breathing in Paleozoic gnathostome fishes. Evolution 28:320325.
Parker R. R., and Black E. C. 1959. Muscular fatigue and mortality in troll-caught chinook salmon (Oncorhynchus tshawytscha). Journal of the Fisheries Resource Board of Canada 16:95106.
Paulik G. J., and De Lacy A. C. 1957. Swimming abilities of upstream migrant silver salmon, sockeye salmon and steelhead at several water velocities. Technical Report 44:140. School of Fisheries, University of Washington, Seattle.
Poupa O., and Lindström L. 1983. Comparative and scaling aspects of heart and body weights with reference to blood supply of cardiac fibers. Comparative biochemistry and physiology 76A:412421.
Rahn H., Rahn K. B., Howell B. J., Gans C., and Tenney S. M. 1971. Air-breathing of the garfish (Lepisosteus osseus). Respiration Physiology 11:285307.
Randall D., Burggren W., Farrell A., and Haswell M. S. 1981. The evolution of air breathing in vertebrates. Cambridge University Press, New York.
Reighard J. 1903. The natural history of Amia calva linnaeus. Pp. 59109In Mark Anniversary Volume. H. Holt, New York.
Roberts T. R. 1972. Ecology of fishes in the Amazon and Congo basins. Bulletin of the Museum of Comparative Zoology 143:117157.
Robertson J. I. 1913. The development of the heart and vascular system of Lepidosiren paradoxa. Quarterly Journal of Microscopical Science 59:53132.
Saksena V. P. 1963. Effects of temperature, light, feeding and activity on the rate of aerial breathing in gar (Lepisosteus). Dissertation Abstracts 24(6):2628. . University of Oklahoma, Norman.
Sanchez-Quintana D., and Hurle J. M. 1987. Ventricular myocardial architecture in marine fishes. Anatomical Record 217:263273.
Santer R. M., and Greer Walker M. 1980. Morphological studies on the ventricle of teleost and elasmobranch hearts. Journal of Zoology, London 190:259272.
Schrenkeisen R. 1963. Field book of fresh-water fishes of North America. Putnam, New York.
Secondat M. 1950. Influence de l'exercice musculaire sur la capacité pour l'oxygène du sang de la carpe (Cyprinus carpio L.). Comptes rendus. Académies des Sciences 230:17871788.
Secondat M., and Diaz D. 1942. Recherches sur la lactacidémie chez le poisson d'eau douce. Académies des Sciences 215:7173.
Shelton G. 1985. Functional and cardiovascular shunts in the amphibia. Pp. 100116In Johansen K. and Burggren W., eds. Alfred Benzon Symposium 21: Cardiovascular shunts; phylogenetic, ontogenetic and clinical aspects. Munksgaard, Copenhagen.
Shelton G., and Burggren W. 1976. Cardiovascular dynamics of the Chelonia during apnea and lung ventilation. Journal of Experimental Biology 64:323343.
Shipman B. 1989. Patterns of ventilation and acid-base recovery following exhausting activity in the air-breathing fish Lepisosteus oculatus. . University of Texas, Arlington.
Shlaifer A., and Breder C. M. 1940. Social and respiratory behavior of small tarpon. Zoologica 25:493512.
Sidell B. D., Driedzic W. R., Stowe D. B., and Johnston I. A. 1987. Biochemical correlations of power development and metabolic fuel preferenda in fish hearts. Physiological Zoology 60:221232.
Sturkie P. D. 1986. Avian physiology, 4th ed.Springer, New York.
Thomson K. S. 1969a. The biology of the lobe-finned fishes. Biological Reviews 44:91154.
Thomson K. S. 1969b. The environment and distribution of Paleozoic sarcopterygian fishes. American Journal of Science 267:457464.
Thomson K. S. 1980. The ecology of Devonian lobe-finned fishes. Pp. 187–122 In Panchen A. L., ed. The terrestrial environment and the origin of land vertebrates. Academic Press, New York.
Tota B., and Gattuso A. 1996. Heart ventricle pumps in teleosts and elasmobranchs: a morphodynamic approach. Journal of Experimental Zoology 275:162171.
Tota B., Cimini V., Salvatore G., and Zummo G. 1983. Comparative study of the ventricular myocardium of elasmobranch and teleost fishes. American Journal of Anatomy 167:1532.
Turner J. D., and Driedzic W. R. 1980. Mechanical and metabolic response of the perfused isolated fish heart to anoxia and acidosis. Canadian Journal of Zoology 58:886889.
Turner J. D., Wood C. M., and Hobe H. 1983. Physiological consequences of severe exercise in the inactive benthic flathead sole Hippoglossoides elassodon: a comparison with the active pelagic rainbow trout Salmo gairdneri. Journal of Experimental Biology 104:269288.
Ultsch G. R. 1996. Gas exchange, hypercarbia and acid-base balance, paleoecology, and the evolutionary transition from water-breathing to air-breathing among vertebrates. Palaeogeography, Palaeoclimatology, Palaeoecology 123:127.
Vorobyeva E. 1975. Some peculiarities in evolution of the rhipidistian fishes. In Lehman J. P., ed. Problèmes actuels de paleontologie. Colloques Internationaux. Centre national de la Recherche scientifique 218:223230.
Walker W. F., and Liem K. F. 1994. Functional anatomy of the vertebrates: an evolutionary perspective. Saunders College, Fort Worth, Tex.
Wasser J. S., Meinertz E. A., Chang S. Y., Lawler R. G., and Jackson D. C. 1992. Metabolic and cardiodynamic responses of isolated turtle hearts to ischemia and reperfusion. American Journal of Physiology 262:R437R443.
West N. H., Butler P. J., and Bevan R. M. 1992. Pulmonary blood flow at rest and during swimming in the green turtle, Chelonia mydas. Physiological Zoology 65:287310.
Wood C. M., Turner J. D., and Graham M. S. 1983. Why do fish die after severe exercise? Journal of Fish Biology 22:189201.
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