Review: Analysis of the evolutionary convergence for high performance swimming in lamnid sharks and tunas.

Elasmobranchs and bony fishes have evolved independently for more than 400 million years. However, two Recent groups, the lamnid sharks (Family Lamnidae) and tunas (Family Scombridae), display remarkable similarities in features related to swimming performance. Traits separating these two groups from other fishes include a higher degree of body streamlining, a shift in the position of the aerobic, red, locomotor muscle that powers sustained swimming to a more anterior location in the body and nearer to the vertebral column, the capacity to conserve metabolic heat (i.e. regional endothermy), an increased gill surface area with a decreased blood-water barrier thickness, a higher maximum blood oxygen carrying capacity, and greater muscle aerobic and anaerobic enzyme activities at in vivo temperatures. The suite of morphological, physiological, and biochemical specializations that define "high-performance fishes" have been extensively characterized in the tunas. This review examines the convergent features of lamnid sharks and tunas in order to gain insight into the extent that comparable environmental selection pressures have led to the independent origin of similar suites of functional characteristics in these two distinctly different taxa. We propose that, despite differences between teleost and elasmobranch fishes, lamnid sharks and tunas have evolved morphological and physiological specializations that enhance their swimming performance relative to other sharks and most other high performance pelagic fishes.

[1]  B. Muir,et al.  Structural Modifications in the Gills of Tunas and Some Other Oceanic Fishes , 1968 .

[2]  J. Teal,et al.  Mako and porbeagle: warm-bodied sharks. , 1969, Comparative biochemistry and physiology.

[3]  J. Mccosker The White Shark, Carcharodon carcharias, Has a Warm Stomach , 1987 .

[4]  R. Shadwick,et al.  Heart rate and stroke volume contribution to cardiac output in swimming yellowfin tuna: response to exercise and temperature. , 1997, The Journal of experimental biology.

[5]  S. Emery,et al.  Hematological Comparisons of Endothermic vs Ectothermic Elasmobranch Fishes , 1986 .

[6]  A. Farrell From Hagfish to Tuna: A Perspective on Cardiac Function in Fish , 1991, Physiological Zoology.

[7]  J. Scharold,et al.  Metabolic rate, heart rate, and tailbeat frequency during sustained swimming in the leopard shark Triakis semifasciata. , 1989, Experimental biology.

[8]  D. Swift The blood haemoglobin concentration of the atlantic mackerel (Scomber scombrus L.) , 1982 .

[9]  K. J. Goldman,et al.  Regulation of body temperature in the white shark, Carcharodon carcharias , 1997, Journal of Comparative Physiology B.

[10]  J. Teal,et al.  Heat conservation in tuna fish muscle. , 1966, Proceedings of the National Academy of Sciences of the United States of America.

[11]  A. Farrell,et al.  Coronary artery reactivity in the mako shark, Isurus oxyrinchus , 1991 .

[12]  Graham,et al.  STUDIES OF TROPICAL TUNA SWIMMING PERFORMANCE IN A LARGE WATER TUNNEL - ENERGETICS , 1994, The Journal of experimental biology.

[13]  J. Morrissey,et al.  Molecular Phylogeny of Elasmobranchs , 1995 .

[14]  F. G. Carey,et al.  Bluefin Tuna Warm Their Viscera During Digestion , 1984 .

[15]  Shadwick,et al.  Muscle strain histories in swimming milkfish in steady and sprinting gaits , 1999, The Journal of experimental biology.

[16]  H. L. Pratt,et al.  Elasmobranchs as living resources: advances in the biology, ecology, systematics, and the status of the fisheries. Proceedings , 1990 .

[17]  S. Wainwright,et al.  Shark Skin: Function in Locomotion , 1978, Science.

[18]  Richard W. Brill,et al.  Selective advantages conferred by the high performance physiology of tunas, billfishes, and dolphin fish , 1996 .

[19]  F. G. Carey,et al.  Daily patterns in the activities of swordfish, Xiphias gladius, observed by acoustic telemetry , 1981 .

[20]  J. R. Brett,et al.  Metabolic Rates and Critical Swimming Speeds of Sockeye Salmon (Oncorhynchus nerka) in Relation to Size and Temperature , 1973 .

[21]  P. W. Hochachka,et al.  Recovery metabolism of skipjack tuna (Katsuwonus pelamis) white muscle: rapid and parallel changes in lactate and phosphocreatine after exercise , 1992 .

[22]  M. Stiassny,et al.  Interrelationships of fishes , 1997 .

[23]  Shadwick,et al.  Muscle dynamics in skipjack tuna: timing of red muscle shortening in relation to activation and body curvature during steady swimming. , 1999, The Journal of experimental biology.

[24]  P. Davie,et al.  Oxygen binding by the blood and hematological effects of capture stress in two big game-fish: mako shark and striped marlin. , 1985, Comparative biochemistry and physiology. A, Comparative physiology.

[25]  P. W. Hochachka,et al.  Structural basis for oxygen delivery: muscle capillaries and manifolds in tuna red muscle. , 1996, Comparative biochemistry and physiology. Part A, Physiology.

[26]  J. Stevens Observations on Reproduction in the Shortfin Mako Isurus oxyrinchus , 1983 .

[27]  C. S. Cavin A Study of the Efficacy of Computer-Simulated Laboratory Experiments. , 1978 .

[28]  K. Holland,et al.  HORIZONTAL AND VERTICAL MOVEMENTS OF YELLOWFIN AND BIGEYE TUNA ASSOCIATED WITH FISH AGGREGATING DEVICES , 1990 .

[29]  Carol A. Stepien,et al.  Molecular systematics of fishes , 1998 .

[30]  Stevens,et al.  Muscle temperature in free-swimming giant Atlantic bluefin tuna (Thunnus thynnus L.). , 2000, Journal of thermal biology.

[31]  A. Farrell,et al.  6 - Hematocrit and Blood Oxygen-Carrying Capacity , 1998 .

[32]  G. Somero,et al.  Partial Characterization of the Buffering Components of the Red and White Myotomal Muscle of Marine Teleosts, with Special Emphasis on Scombrid Fishes , 1987, Physiological Zoology.

[33]  F. Koehrn,et al.  Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to locomotion and endothermy , 1983 .

[34]  Q. Bone,et al.  Vascularization of the lateral muscle of some elasmobranchiomorph fishes , 1981 .

[35]  H. Dewar,et al.  ASPECTS OF SHARK SWIMMING PERFORMANCE DETERMINED USING A LARGE WATER TUNNEL , 1990 .

[36]  F. G. Carey A brain heater in the swordfish. , 1982, Science.

[37]  K. Dickson,et al.  Biochemical indices of aerobic and anaerobic capacity in muscle tissues of California elasmobranch fishes differing in typical activity level , 1993 .

[38]  H. Dewar,et al.  Tuna aerobic swimming performance: Physiological and environmental limits based on oxygen supply and demand , 1996 .

[39]  Graham,et al.  Red muscle activation patterns in yellowfin (Thunnus albacares) and skipjack (Katsuwonus pelamis) tunas during steady swimming. , 1999, The Journal of experimental biology.

[40]  B. Block Endothermy in fish: thermogenesis, ecology and evolution , 1991 .

[41]  Graham,et al.  STUDIES OF TROPICAL TUNA SWIMMING PERFORMANCE IN A LARGE WATER TUNNEL - THERMOREGULATION , 1994, The Journal of experimental biology.

[42]  T. Gleeson,et al.  Post-exercise lactate metabolism: a comparative review of sites, pathways, and regulation. , 1996, Annual review of physiology.

[43]  B. Block Structure of the brain and eye heater tissue in marlins, sailfish, and spearfishes , 1986, Journal of morphology.

[44]  III. – MYOTOMAL MUSCLE FIBER TYPES IN SCOMBER AND KATSUWONUS , 1978 .

[45]  Jones,et al.  Blood volume, plasma volume and circulation time in a high-energy-demand teleost, the yellowfin tuna (Thunnus albacares) , 1998, The Journal of experimental biology.

[46]  Alternative life-history styles of cartilaginous fishes in time and space , 1990 .

[47]  L. Compagno Relationships of the megamouth shark, Megachasma pelagios (Lamniformes, Megachasmidae), with comments on its feeding habits , 1990 .

[48]  D. Holts,et al.  Horizontal and vertical movements of the shortfin mako shark, Isurus oxyrinchus, in the southern California bight. , 1993 .

[49]  Q. Bone,et al.  The retial system of the locomotor muscles in the thresher shark , 1983, Journal of the Marine Biological Association of the United Kingdom.

[50]  J. Graham,et al.  Hemodynamics and Blood Properties of the Shortfin Mako Shark (Isurus oxyrinchus) , 1997 .

[51]  C. C. Lindsey 1 - Form, Function, and Locomotory Habits in Fish , 1978 .

[52]  S. Shirai Chapter 2 – Phylogenetic Interrelationships of Neoselachians (Chondrichthyes: Euselachii) , 1996 .

[53]  P. Gilbert,et al.  Sharks, Skates, and Rays , 1967 .

[54]  P. Bushnell,et al.  2 - The Arterial System , 1992 .

[55]  R. Shadwick,et al.  Muscle Dynamics in Fish During Steady Swimming , 1998 .

[56]  C. R. Taylor,et al.  A companion to Animal physiology , 1982 .

[57]  Wolfgang H Berger,et al.  Ocean productivity and paleoproductivity - an overview , 1989 .

[58]  Muscles and Locomotion , 1988 .

[59]  K. Dickson Locomotor muscle of high-performance fishes: What do comparisons of tunas with ectothermic sister taxa reveal? , 1996 .

[60]  Robert E. Shadwick,et al.  8. Swimming and muscle function , 2001 .

[61]  J. Wittenberg,et al.  Myoglobin-facilitated oxygen diffusion: role of myoglobin in oxygen entry into muscle. , 1970, Physiological reviews.

[62]  Kenneth D. Lawson,et al.  Warm-Bodied Fish , 1971 .

[63]  J. R. Brett,et al.  Metabolic Rate and Energy Expenditure of the Spiny Dogfish, Squalus acanthias , 1978 .

[64]  A. Dizon,et al.  The physiological ecology of tunas , 1979 .

[65]  C. Franklin,et al.  Cardiac physiology in tunas. I. In vitro perfused heart preparations from yellowfin and skipjack tunas , 1992 .

[66]  J. Teal,et al.  The Visceral Temperatures of Mackerel Sharks (Lamnidae) , 1981, Physiological Zoology.

[67]  H. L. Pratt,et al.  Age and growth of the shortfin Mako, Isurus oxyrinchus, using four methods , 1983 .

[68]  C. Milligan,et al.  Metabolic recovery from exhaustive exercise in rainbow trout , 1996 .

[69]  F. G. Carey,et al.  Regulation of brain and eye temperatures by the bluefin tuna. , 1972, Comparative biochemistry and physiology. A, Comparative physiology.

[70]  David H. Evans,et al.  The Physiology of Fishes , 1994 .

[71]  C. Emiliani The oceanic lithosphere , 1981 .

[72]  J. Maisey Higher elasmobranch phylogeny and biostratigraphy , 1984 .

[73]  Q. Bone,et al.  Mechanics and Physiology of Animal Swimming: Contributors , 1994 .

[74]  J. Teal,et al.  Regulation of body temperature by the bluefin tuna. , 1969, Comparative biochemistry and physiology.

[75]  Catalase Activity in the Epidermis of Patients with Advanced Cancer , 1964, Nature.

[76]  T. Flatmark,et al.  The myoglobin content in red, intermediate and white fibres of the swimming muscle sin three species of shark–a comparative study using high‐performance liquid chromatography , 1981 .

[77]  R. Shadwick,et al.  Oxygen transport and cardiovascular responses to exercise in the yellowfin tuna Thunnus albacares. , 1997, The Journal of experimental biology.

[78]  J. Graham,et al.  Physiological Thermoregulation in the Albacore Thunnus alalunga , 1981, Physiological Zoology.

[79]  F. Fry,et al.  Brain and muscle temperatures in ocean caught and captive skipjack tuna , 1971 .

[80]  R. Burne Some Peculiarities of the Blood-Vascular System of the Porbeagle Shark (Lamna Cornubica) , 1924 .

[81]  H. L. Pratt,et al.  Temperature and Activities of a White Shark, Carcharodon carcharias , 1982 .

[82]  S. Egginton,et al.  Comparative rheology of human and trout red blood cells. , 1993, The Journal of experimental biology.

[83]  CHAPTER 5 – Evolutionary Relationships of the White Shark: A Phylogeny of Lamniform Sharks Based on Dental Morphology , 1996 .

[84]  J. Magnuson COMPARATIVE STUDY OF ADAPTATIONS FOR CONTINUOUS SWIMMING AND HYDROSTATIC EQUILIBRIUM OF SCOMBROID AND XIPHOID FISHES , 1973 .

[85]  V. Bhargava,et al.  Mechanisms of venous return and ventricular filling in elasmobranch fish. , 1996, The American journal of physiology.

[86]  R. L. Alexander Blood supply to the eyes and brain of lamniform sharks (Lamniformes) , 1998 .

[87]  P. W. Hochachka,et al.  Mitochondrial metabolism of cardiac and skeletal muscles from a fast (Katsuwonus pelamis) and a slow (Cyprinus carpio) fish , 1992 .

[88]  J. R. Brett The Relation of Size to Rate of Oxygen Consumption and Sustained Swimming Speed of Sockeye Salmon (Oncorhynchus nerka) , 1965 .

[89]  J. L. Roberts II. – RAM GILL VENTILATION IN FISH , 1978 .

[90]  M. Levine Great White Sharks , 1998 .

[91]  A. Maresca,et al.  Cardiac growth, myoglobin, proteins and DNA in developing tuna (Thunnus thynnus thynnus L.) , 1981 .

[92]  J. Finnerty,et al.  Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny. , 1993, Science.

[93]  G. M. Hughes,et al.  Gill Dimensions for Three Species of Tunny , 1969 .

[94]  E. Duursma Productivity of the ocean: Present and past: Edited by W.H. Berger, V.S. Smetacek and G. Wefer. John Wiley & Sons, Chichester, UK 1989. A Dahlem Workshop Report, Life Sciences Research Rep. 44. xiii + 471 pp. ISBN 0-471-92246-3 , 1992 .

[95]  J. Macdougall A Short History of Planet Earth: Mountains, Mammals, Fire, and Ice , 1996 .

[96]  C. Mangano,et al.  Ventricle morphology in pelagic elasmobranch fishes. , 1985, Comparative biochemistry and physiology. A, Comparative physiology.

[97]  B. Block Billfish Brain and Eye Heater: A New Look at Nonshivering Heat Production , 1987 .

[98]  P. W. Hochachka,et al.  Metabolic sources of heat and power in tuna muscles. II. Enzyme and metabolite profiles. , 1979, The Journal of experimental biology.

[99]  W. Berger,et al.  Paleoceanography — the Deep-Sea Record , 1993 .

[100]  J. Graham,et al.  The evolution of thunniform locomotion and heat conservation in scombrid fishes: New insights based on the morphology of Allothunnus fallai , 2000 .

[101]  R. Smith,et al.  Body temperature of the salmon shark, Lamna ditropis , 1983, Journal of the Marine Biological Association of the United Kingdom.

[102]  T. Shuttleworth Physiology of Elasmobranch Fishes , 1988, Springer Berlin Heidelberg.

[103]  J. Altringham,et al.  Why do tuna maintain elevated slow muscle temperatures? Power output of muscle isolated from endothermic and ectothermic fish. , 1997, The Journal of experimental biology.

[104]  F. G. Carey,et al.  Temperature regulation in free-swimming bluefin tuna. , 1973, Comparative biochemistry and physiology. A, Comparative physiology.

[105]  Andrew P. Martin,et al.  Rates of mitochondrial DNA evolution in sharks are slow compared with mammals , 1992, Nature.

[106]  Graham,et al.  STUDIES OF TROPICAL TUNA SWIMMING PERFORMANCE IN A LARGE WATER TUNNEL - KINEMATICS , 1994, The Journal of experimental biology.

[107]  Q. Bone 6 Locomotor Muscle , 1978 .

[108]  P. Bushnell,et al.  The metabolic rate of an active, tropical elasmobranch, the lemon shark (Negaprion brevirostris). , 1989, Experimental biology.

[109]  D. Sánchez-Quintana,et al.  Ventricular myocardial architecture in marine fishes , 1987, The Anatomical record.

[110]  K. Dickson,et al.  Maximum sustainable speeds and cost of swimming in juvenile kawakawa tuna (Euthynnus affinis) and chub mackerel (Scomber japonicus). , 2000, The Journal of experimental biology.

[111]  C. A. Pell,et al.  The horizontal septum: Mechanisms of force transfer in locomotion of scombrid fishes (Scombridae, Perciformes) , 1993, Journal of morphology.

[112]  J. Maisey Relationships of the megamouth shark, Megachasma , 1985 .

[113]  M. Lighthill Aquatic animal propulsion of high hydromechanical efficiency , 1970, Journal of Fluid Mechanics.

[114]  P. W. Hochachka,et al.  Metabolic sources of heat and power in tuna muscles. I. Muscle fine structure. , 1979, The Journal of experimental biology.

[115]  J. Harvey,et al.  Preliminary studies on the age and growth of blue (Prionace glauca), common thresher (Alopias vulpinus), and shortfin mako (Isurus oxyrinchus) sharks from California waters , 1983 .

[116]  B. Collette,et al.  Systematics and morphology of the bonitos (Sarda) and their relatives (Scombridae, Sardini) , 1975 .

[117]  L. Rome,et al.  Contraction dynamics and power production of pink muscle of the scup (Stenotomus chrysops). , 1996, The Journal of experimental biology.

[118]  J. Stevens,et al.  Sharks and Rays of Australia , 1991 .

[119]  W. H. Neill,et al.  Respiration rates and low-oxygen tolerance limits in skipjack tuna , 2013 .

[120]  David G. Ainley,et al.  Great white sharks : the biology of Carcharodon carcharias , 1996 .

[121]  J. M. Donley,et al.  Swimming kinematics of juvenile kawakawa tuna (Euthynnus affinis) and chub mackerel (Scomber japonicus). , 2000, The Journal of experimental biology.

[122]  Andrew P. Martin,et al.  CHAPTER 13 – Interrelationships of Lamniform Sharks: Testing Phylogenetic Hypotheses with Sequence Data , 1997 .

[123]  J. Mcleese,et al.  Why bluefin tuna have warm tummies: temperature effect on trypsin and chymotrypsin. , 1984, The American journal of physiology.

[124]  S. Applegate,et al.  CHAPTER 4 – The Fossil History of Carcharodon and Its Possible Ancestor, Cretolamna: A Study in Tooth Identification , 1996 .

[125]  K. Kishinouye Contributions to the comparative study of the so-called scombroid fishes , 1923 .

[126]  R. Shabetai,et al.  Elevated pericardial pressure and cardiac output in the leopard shark Triakis semifasciata during exercise: the role of the pericardioperitoneal canal , 1989 .

[127]  John J. Magnuson,et al.  Hydrostatic Equilibrium of Euthynnus affinis, a Pelagic Teleost Without a Gas Bladder , 1970 .

[128]  B. Collette II. – ADAPTATIONS AND SYSTEMATICS OF THE MACKERELS AND TUNAS , 1978 .

[129]  G. Zummo,et al.  Comparative study of the arterial and lacunary systems of the ventricular myocardium of elasmobranch and teleost fishes. , 1983, The American journal of anatomy.

[130]  C. Lowe Bioenergetics and swimming efficiency of juvenile scalloped hammerhead sharks, Sphyrna lewini, in Kaneohe Bay, Oahu, Hawaii , 1998 .

[131]  M. Greek-Walker,et al.  A survey of red and white muscle in marine fish , 1975 .

[132]  K. Yano Biology of the megamouth shark , 1997 .

[133]  J. Maisey Chondrichthyan phylogeny: a look at the evidence , 1984 .

[134]  H. Dewar,et al.  The aerobic capacity of tunas: Adaptation for multiple metabolic demands , 1996 .

[135]  D. Ellerby,et al.  Slow muscle function of Pacific bonito (Sarda chiliensis) during steady swimming. , 2000, The Journal of experimental biology.

[136]  P. Bushnell,et al.  Metabolic and cardiac scope of high energy demand teleosts, the tunas , 1991 .

[137]  Hughes Gm Morphological measurements on the gills of fishes in relation to their respiratory function. , 1970 .

[138]  Robert L. Carroll,et al.  Vertebrate Paleontology and Evolution , 1988 .

[139]  David A. Fournier,et al.  Physiological and behavioural thermoregulation in bigeye tuna (Thunnus obesus) , 1992, Nature.

[140]  B. Collette,et al.  Unstable and Stable Classifications of Scombroid Fishes , 1995 .

[141]  Barbara A. Block,et al.  Horizontal movements and depth distribution of large adult yellowfin tuna (Thunnus albacares) near the Hawaiian Islands, recorded using ultrasonic telemetry: implications for the physiological ecology of pelagic fishes , 1999 .

[142]  A. Szczepanski,et al.  GILL DIMENSIONS IN PELAGIC ELASMOBRANCH FISHES , 1986 .

[143]  R. Brill,et al.  Thermoregulation in Tunas , 1979 .

[144]  Robert L. Carroll,et al.  Patterns and Processes of Vertebrate Evolution , 1997 .

[145]  Harry L. Fierstine,et al.  Measurements of Swimming Speeds of Yellowfin Tuna and Wahoo , 1964, Nature.

[146]  A. K. Morgan,et al.  Physiological stress responses in big gamefish after capture: observations on plasma chemistry and blood factors. , 1986, Comparative biochemistry and physiology. A, Comparative physiology.

[147]  F. G. Carey,et al.  One why of the warmth of warm-bodied fish. , 1981, The American journal of physiology.

[148]  P. W. Hochachka,et al.  Capillary–fiber geometrical relationships in tuna red muscle , 1992 .

[149]  Thomas D. Williams,et al.  Archival tagging of Atlantic bluefin tuna (Thunnus thynnus thynnus) , 1998 .

[150]  R. Shadwick,et al.  High-speed swimming: Enhanced power in yellowfin tuna , 2001, Nature.

[151]  B. Block,et al.  Orbital rete and red muscle vein anatomy indicate a high degree of endothermy in the brain and eye of the salmon shark , 2001 .

[152]  B. Ely,et al.  Orthodox and unorthodox phylogenetic relationships among tunas revealed by the nucleotide sequence analysis of the mitochondrial DNA control region , 1997 .

[153]  G. M. Hughes 1 General Anatomy of the Gills , 1984 .