Functional Genomics and the Comparative Physiology of Hypoxia

Annual Review of Physiology

Volumn 65, Issue , 2003, Pages 203-230

  Powell, Frank L ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Adaptation; Artificial selection; Evolution; Phylogeny; Systems biology

Indexed keywords

OXYGEN;

ADAPTATION; ALTITUDE; ASCITES; BREATHING PATTERN; ECOLOGY; EVOLUTION; EVOLUTIONARY ADAPTATION; EXPRESSED SEQUENCE TAG; GENE DELETION; GENE EXPRESSION; GENOMICS; HUMAN; HYPOXIA; LUNG VENTILATION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PULMONARY HYPERTENSION; REVIEW; RODENT; TRANSGENIC MOUSE; ANIMAL; ANOXIA; COMPARATIVE STUDY; GENETICS; PATHOPHYSIOLOGY; SPECIES DIFFERENCE;

ANIMALS; ANOXIA; GENOMICS; HUMANS; PHYLOGENY; SPECIES SPECIFICITY;

EID: 0037974523     PISSN: 00664278     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.physiol.65.092101.142711     Document Type: Review

References (144)

1. McKusick VA. 1997. Genomics: structural and functional studies of genomes. Genomics 45:244-49
2. Hieter P, Boguski M. 1997. Functional genomics: It's all how you read it. Science 278:601-2
3. Krebs HA. 1975. The August Krogh Principle: "For many problems there is an animal on which it can be most conveniently studied." J. Exp. Zool. 194:221-26
4. Bennett AF. 1987. The accomplishments of ecological physiology. In New Directions in Ecological Physiology, ed. ME Feder, AF Bennett, RB Huey, WW Burggren, pp. 1-8. New York: Cambridge Univ. Press
5. Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm. A critique of the adaptationist program. Proc. R. Soc. London Ser. B 205B:581-98
6. Garland T, Adolph SC. 1994. Why not to do two species comparisons - limitations on inferring adaptation. Physiol. Zool. 67:797-828
7. Feder ME, Bennett AF, Huey RB. 2000. Evolutionary physiology. Annu. Rev. Ecol. Syst. 31:315-41
8. 2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 15:551-78
9. Semenza GL. 2000. HIF-1: the mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88:1474-80
10. Zhu H, Bunn HF. 1999. Oxygen sensing and signaling: impact on the regulation of physiologically important genes. Respir. Physiol. 115:239-48
11. 2 sensing. Science 292:464-68
12. 2-regulated prolyl hydroxylation. Science 292:468-72
13. Jiang H, Guo R, Powell-Coffman JA. 2001. The Caenorhabditis elegans HIF-1 gene encodes a bHLH-PAS protein that is required for adaptation to hypoxia. Proc. Natl. Acad. Sci. USA 98:7916-21
14. Banfield JF, Marshall CR. 2000. Genomics and the geosciences. Science 287:605-6
15. Gracey AY, Cossins AR. 2003. Application of microarray technology in environmental and comparative physiology. Annu. Rev. Physiol. 65:231-59
16. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D. 2002. Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868-72
17. Marth JD. 1996. Recent advances in gene mutagenesis by site-directed recombination. J. Clin. Invest. 97:1999-2002
18. Kline DD, Yang T, Premkumar DR, Thomas AJ, Prabhakar N. 2000. Blunted respiratory responses to hypoxia in mutant mice deficient in nitric oxide synthase-3. J. Appl. Physiol. 88:1496-508
19. Erickson JT, Conover JC, Borday V, Champagnat J, Barbacid M, et al. 1996. Mice lacking brain-derived neurotrophic factor exhibit visceral sensory neuron losses distinct from mice lacking NT4 and display a severe developmental deficit in control of breathing. J. Neurosci. 16:5361-71
20. Burnet H, Bevengut M, Chakri F, Bou-Flores C, Coulon P, et al. 2001. Altered respiratory activity and respiratory regulations in adult monoamine oxidase A-deficient mice. J. Neurosci. 21:5212-21
21. 2a-adrenergic receptors. Adv. Exp. Med. Biol. 499:201-8
22. Kuwaki T, Cao WH, Kurihara Y, Kurihara H, Ling GY, et al. 1996. Impaired ventilatory responses to hypoxia and hypercapnia in mutant mice deficient in endothelin-1. Am. J. Physiol. Regul. Integr. Comp. Physiol. 270:R1279-R86
23. i and respiratory responses to hypoxia. Brain Res. 872:188-93
24. Rozanov C, Roy A, Mokashi A, Daudu P, Ross C, Lahiri S. 2001. Inhibition or lack of NAD(P)H oxidase subunits does not alter the normal cytosolic calcium, sensory and respiratory response of chemoreceptors. Adv. Exp. Med. Biol. 499:67-72
25. Powell FL, Milsom WK, Mitchell GS. 1998. Time domains of the hypoxic ventilatory response. Respir. Physiol. 112:123-34
26. Huey KA, Low MJ, Kelly MA, Juarez R, Szewczak JM, Powell FL. 2000. Ventilatory responses to acute and chronic hypoxia in mice: effects of dopamine D-2 receptors. J. Appl. Physiol. 89:1142-50
27. Kline DD, Overholt JL, Prabhakar NR. 2002. Mutant mice deficient in NOS-1 exhibit attenuated long-term facilitation and short-term potentiation in breathing. J. Physiol. 539:309-15
28. Fan G, Siniaia M, Poon CS, Jaenisch R. 2001. Effect of DNA hypomethylation on neural control of respiration: a genetic model. Adv. Exp. Med. Biol. 499:195-200
29. Fan G, Beard C, Chen RZ, Csankovszki G, Sun Y, et al. 2001. DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J. Neurosci. 21:788-97
30. Markstahler U, Kremer E, Kimmina S, Becker K, Richter DW. 2002. Effects of functional knock-out of α1 glycine-receptors on breathing movements in oscillator mice. Respir. Physiol. Neurobiol. 130:33-42
31. Poon CS, Zhou Z, Champagnat J. 2000. NMDA receptor activity in utero averts respiratory depression and anomalous long-term depression in newborn mice. J. Neurosci. 20:RC73:1-6
32. Bermingham JR, Scherer SS, OConnell S, Arroyo E, Kalla KA, et al. 1996. Tst-1/Oct-6/SCIP regulates a unique step in peripheral myelination and is required for normal respiration. Genes Dev. 10:1751-62
33. Yu AY, Shimoda LA, Iyer NV, Huso DL, Sun X, et al. 1999. Impaired physiological responses to chronic hypoxia in mice partially deficient for hypoxia-inducible factor 1α. J. Clin. Invest. 103:691-96
34. Yuan X, Goldman WF, Tod ML, Rubin LJ, Blaustein MP. 1993. Hypoxia reduces potassium currents in cultured rat pulmonary but not mesenteric arterial myocytes. Am. J. Physiol. Lung Cell Mol. Physiol. 264:L116-L23
35. Tankersley CG, Fitzgerald RS, Kleeberger SR. 1994. Differential control of ventilation among inbred strains of mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 267:R1371-R77
36. Tankersley CG, Fitzgerald RS, Levitt RC, Mitzner WA, Ewart SL, Kleeberger SR. 1997. Genetic control of differential baseline breathing pattern. J. Appl. Physiol. 82:874-81
37. Tankersley CG, Elston RC, Schnell AH. 2000. Genetic determinants of acute hypoxic ventilation: patterns of inheritance in mice. J. Appl. Physiol. 88:2310-18
38. Tankersley CG. 2000. A genomic model for differential hypoxic ventilatory responses. Adv. Exp. Med. Biol. 475:75-85
39. Tankersley CG, Rabold R, Mitzner W 1999. Differential lung mechanics are genetically determined in inbred murine strains. J. Appl. Physiol. 86:1764-69
40. Tankersley CG, DiSilvestre DA, Jedlicka AE, Wilkins HM, Zhang L. 1998. Differential inspiratory timing is genetically linked to mouse chromosome 3. J. Appl. Physiol. 85:360-65
41. Tankersley CG, Kulaga H, Wang MM. 2001. Inspiratory timing differences and regulation of Gria2 gene variation: a candidate gene hypothesis. Adv. Exp. Med. Biol. 499:477-82
42. Tankersley CG. 2001. Variation in acute hypoxic ventilatory response is determined by a quantitative trait locus on mouse chromosome 9. J. Appl. Physiol. 90:1615-22
43. Olson EB Jr, Bonne CJ, Dwinell MR, Podolsky A, Virdruk EH, et al. 2001. Ventilatory long-term facilitation in unanesthesized rats. J. Appl. Physiol. 91:709-16
44. Powell FL, Huey KA, Dwinell MR. 2000. Central nervous system mechanisms of ventilatory acclimatization to hypoxia. Respir. Physiol. 121:223-36
45. Silver LM. 1995. Mouse Genetics: Concepts and Applications. New York: Oxford Univ. Press
46. Soutiere SE, Tankersley CG. 2001. Challenges implicit to gene discovery research in the control of ventilation during hypoxia. High Alt. Med. Biol. 2:191-200
47. Jacob HJ, Brown DM, Bunker RK, Daly MJ, Dzau VJ, et al. 1995. A genetic linkage map of the laboratory rat, Rattus norvegicus. Nat. Genet. 9:63-69
48. Han F, Strohl KP. 2000. Inheritance of ventilatory behavior in rodent models. Respir. Physiol. 121:247-56
49. Strohl KP, Thomas AJ, St. Jean P, Schlenker EH, Koletsky RJ, Schork NJ. 1997. Ventilation and metabolism among rat strains. J. Appl. Physiol. 82:317-23
50. Subramanian S, Han F, Erokwu BO, Dick TE, Strohl KP. 2001. Do genetic factors influence the Dejours phenomenon? Adv. Exp. Med. Biol. 499:209-14
51. Stoll M, Cowley AW Jr, Tonellato PJ, Greene AS, Kaldunski ML, et al. 2001. A genomic-systems biology map for cardiovascular function. Science 294:1723-26
52. Hodges M, Forster HV, Cowley AW Jr, Jacob HJ, et al. 2000. Differences in ventilatory response to hypoxia and hypercapnia among three inbred strains of adult rats. FASEB J. 14:A640 (Abstr.)
53. Dwinell MR, Forster HV, Hodges M, Cowley AW. 2002. Hypercapnic ventilatory responses in inbred parental and consomic strains of adult rats. FASEB J. 14:A879 (Abstr.)
54. Brown PO, Botstein D. 1999. Exploring the new world of the genome with DNA microarrays. Nat. Genet. 21:33-37
55. Gracey AY, Troll JV, Somero GN. 2001. Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc. Natl. Acad. Sci. USA 98:1993-98
56. 2+ concentrations. J. Exp. Biol. 201:1141-52
57. Hochachka PW. 1986. Defense strategies against hypoxia and hypothermia. Science 231:234-41
58. Aguilar NM. 2000. Comparative physiology of air-breathing gobies. PhD thesis. Univ. Calif., San Diego. 201 pp.
59. Tucker VA. 1972. Respiration during flight in birds. Respir. Physiol. 14:75-82
60. Swan LW 1970. Goose of the Himalayas. Nat. Hist. 79:68-75
61. Butler PJ. 1991. Exercise in birds. J. Exp. Biol. 160:233-62
62. Jessen TH, Weber RE, Fermi G, Tame J, Braunitzer G. 1991. Adaptation of bird hemoglobins to high altitudes: demonstration of molecular mechanism by protein engineering. Proc. Natl. Acad. Sci. USA 88:6519-22
63. Golding GB, Dean AM. 1998. The structural basis of molecular adaptation. Mol. Biol. Evol. 15:355-69
64. Hochachka PW, Somero GN. 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford, UK: Oxford Univ. Press. 466 pp.
65. Szentivanyi M Jr, Zou AP, Mattson DL, Soares P, Moreno C, et al. 2002. Renal medullary nitric oxide deficit of Dah1 S rats enhances hypertensive actions of angiotensin II. Am. J. Physiol. Regul. Integr. Comp. Physiol. 283:R266-R72
66. Rose MR, Graves JL, Hutchison EW. 1990. The use of selection to probe patterns of pleiotropy in fitness characters. In Insect Life Cycles: Genetics, Evolution and Co-Ordination, ed. F Gilbert, pp. 29-42. New York: Springer Verlag
67. Bennett AF, Lenski RE. 1999. Experimental evolution and its role in evolutionary physiology. Am. Zool. 39:346-62
68. Garland T Jr. 2001. Phylogenetic comparison and artificial selection. Two approaches in evolutionary physiology. Adv. Exp. Med. Biol. 502:107-32
69. Koch LG, Britton SL. 2001. Artificial selection for intrinsic aerobic endurance running capacity in rats. Physiol. Genet. 5:45-52
70. Hussain SO, Barbato JC, Koch LG, Metting PJ, Britton SL. 2001. Cardiac function in rats selectively bred for low- and high-capacity running. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R1787-R91
71. Ideker T, Galitski T, Hood L. 2001. A new approach to decoding life: systems biology. Annu. Rev. Genom. Hum. Genet. 2:343-72
72. Cowley AW Jr. 1999. The emergence of physiological genomics. J. Vasc. Res. 36:83-90
73. Kitano H. 2002. Systems biology: a brief overview. Science 295:1662-64
74. Davidson EH, Rast JP, Oliveri P, Ransick A, Calestani C, et al. 2002. A genomic regulatory network for development. Science 295:1669-78
75. Guet CC, Elowitz MB, Hsing W, Leibler S. 2002. Combinatorial synthesis of genetic networks. Science 296:1466-70
76. Hochachka PW, Mottishaw PD. 1998. Evolution and adaptation of the diving response: Phocids and Otariids. In Cold Ocean Symposia, ed. HO Pörtner, RC Playle, pp. 391-431. Cambridge, UK: Cambridge Univ. Press
77. Mottishaw PD, Thornton S, Hochachka PW 1999. The diving resonse and its surprising evolutionary path in seals and sea lions. Am. Zool. 39:434-50
78. Butler PJ, Jones DR. 1997. Physiology of diving of birds and mammals. Physiol. Rev. 77:837-99
79. Dunmire WW. 1960. An altitudinal survey of reproduction in Peromyscus maniculatus. Ecology 41:174-82
80. Hayes JP, O'Connor CS. 1999. Natural selection on thermogenic capacity of high-altitude deer mice. Evolution 53:1280-87
81. MacMillen RE, Garland T. 1989. Adaptive physiology. In Advances in the Study of Peromyscus (Rodentia), ed. GL Kirkland, JN Layne, pp. 143-68. Lubbock, TX: Texas Tech Univ. Press
82. Snyder LRG. 1981. Deer mouse hemoglobins: Is there genetic adaptation to high altitude? BioScience 31:299-304
83. Chappell MA, Snyder LRG. 1984. Biochemical and physiological correlates of deer mouse α-chain hemoglobin polymorphisms. Proc. Natl. Acad. Sci. USA 81:5484-88
84. Snyder LRG, Hayes JP, Chappell MA. 1998. Alpha-chain hemoglobin polymorphisms are correlated with altitude in the deer mouse, Peromyscus maniculatus. Evolution 42:689-97
85. Chappell MA, Hayes JP, Snyder LRG. 1988. Hemoglobin polymorphisms in deer mice (Peromyscus maniculatus): physiology of beta-globin variants and alpha-globin recombinants. Evolution 42:681-88
86. Hammond KA, Szewczak JM, Krol E. 2001. Effects of altitude and temperature on organ phenotypic plasticity along an altitudinal gradient. J. Exp. Biol. 204:1991-2000
87. Hammond KA, Kristan DM. 2000. Responses to lactation and cold exposure by deer mice (Peromyscus maniculatus). Physiol. Biochem. Zool. 73:547-56
88. Hock RJ. 1961. Effect of altitude on endurance running. J. Appl. Physiol. 16:435-38
89. Hock RJ. 1964. Physiological responses of deer mice to various native altitudes. In The Physiological Effects of High Altitude, ed. WH Weihe, pp. 59-72. New York: MacMillan
90. O'Connor CS, Hayes JP, St. Jeor SC. 1997. Sin Nombre virus does not impair respiratory function of wild deer mice. J. Mammol. 78:661-68
91. Rowe JE, St. Jeor SC, Riolo J, Otteson EW, Monroe MC, et al. 1995. Coexistence of several novel hanta viruses in rodents indigenous to North America. Virology 213:122-30
92. Dewey MJ, Dawson WD. 2001. Deer mice: "The Drosophila of North American mammalogy." Genesis 29:105-9
93. Hopkins SR, Powell FL. 2001. Common themes of adaptation to hypoxia. Adv. Exp. Med. Biol. 502:153-67
94. Poyart C, Wajcman H, Kister J. 1992. Molecular adaptation of hemoglobin function in mammals. Respir. Physiol. 90:3-17
95. 2 affinity of animals living at high altitude. J. Appl. Physiol. 42:139-43
96. Rahn H. 1966. Aquatic gas exchange: theory. Respir. Physiol. 1:1-12
97. Ward MP, Milledge JS, West JB. 2000. High Altitude Medicine and Physiology. London: Arnold. 434 pp.
98. Hurson MJ, Greene HM, Szewczak JM, Wickler SJ. 2002. 2,3-DPG changes in horses, mules and burros with exposure to altitude. Physiologist 45:376
99. 2 content and catecholamine levels during hypoxia in rainbow trout and American eel. Am. J. Physiol. Regul. Integr. Comp. Physiol. 263:R240-R49
100. Glover G, Newsom I. 1915. Dropsy of high altitudes. Colo. Agric. Exp. Sta. Bull. 204:3-24
101. Bisgard GE. 1977. Pulmonary hypertension in cattle. Adv. Vet. Sci. Comp. Med. 21:151-72
102. Will DH, Hicks JL, Card CS, Alexander AF. 1975. Inherited susceptibility of cattle to high-altitude pulmonary hypertension. J. Appl. Physiol. 38:491-94
103. Weir EK, Tucker A, Reeves JT. 1974. The genetic factor influencing pulmonary hypertension in cattle at high altitude. Cardiovasc. Res. 8:745-49
104. Cruz JC, Reeves JT, Russell BE, Alexander AF, Will DH. 1980. Embryo transplanted calves: the pulmonary hypertensive trait is genetically transmitted. Proc. Soc. Exp. Biol. Med. 164:142-45
105. Holt TN, Ramirez G. 1998. Genetic adaptation of cattle to high altitude. Am. Zool. 38:10A (Abstr.)
106. Fagan KA, Weil JV. 2001. Potential genetic contributions to control of the pulmonary circulation and ventilation at high altitude. High Alt. Med. Biol. 2:165-71
107. Julian RJ. 1993. Ascites in poultry. Avian Pathol. 23:419-54
108. Black CP, Tenney SM. 1980. Oxygen transport during progressive hypoxia in high-altitude and sea-level waterfowl. Respir. Physiol. 39:217-39
109. Holle JP, Heisler N, Scheid P. 1978. Blood flow distribution in the duck lung and its control by respiratory gases. Am. J. Physiol. 234:R146-R54
110. Powell FL, Hastings RH, Mazzone RW. 1985. Pulmonary vascular resistance during unilateral pulmonary arterial occlusion in ducks. Am. J. Physiol. Regul. Integr. Comp. Physiol. 249:R39-R43
111. Powell FL. 2000. Respiration. In Sturkie's Avian Physiology, ed. GC Whittow, pp. 233-64. San Diego: Academic
112. Burton RR, Smith AH. 1967. Effect of polycythemia and chronic hypoxia on heart mass in the chicken. J. Appl. Physiol. 22:782-85
113. Peacock AJ, Pickett C, Morris K, Reeves JT. 1990. Spontaneous hypoxaemia and right ventricular hypertrophy in fast growing broiler chickens reared at sea level. Comp. Biochem. Physiol. 97A:537-41
114. Maina JN, King AS, Settle G. 1989. An allometric study of pulmonary morphometric parameters in birds, with mammalian comparisons. Philos. Trans. R. Soc. London Ser. B 326:1-57
115. Diamond JM. 1998. Evolution of biological safety factors: a cost/benefit analysis. In Principles of Animal Design: The Optimization and Symmorphosis Debate, ed. ER Weibel, CR Taylor, L Bolis, pp. 21-27. Cambridge, UK: Cambridge Univ. Press
116. Mejia O, Leon-Velarde F, Monge C. 1994. The effect of inositol hexaphosphate in the high-affinity hemoglobin of the Andean chicken (Gallus gallus). Comp. Biochem. Physiol. B 109:437-11
117. Smith AC, Abplanalp H, Harwood LM, Kelly CF. 1959. Poultry at high altitude. Calif. Agric. 13:8-9
118. Erickson BK, Erickson HH, Coffman JR. 1990. Pulmonary artery, aortic and oesophageal pressure changes during high intensity treadmill exercise in the horse: a possible relation to exercise-induced pulmonary haemorrhage. Equine Vet. J. Suppl. June(9):47-52
119. Seaman J, Erickson BK, Kubo K, Hiraga A, Kai M, et al. 1995. Exercise induced ventilation/perfusion inequality in the horse. Equine Vet. J. 27:104-9
120. 2max. J. Appl. Physiol. 66:2491-95
121. 2 difference by helium breathing in the exercising horse. J. Appl. Physiol. 76:2794-801
122. Brutsaert TD. 2001. Limits on inferring genetic adaptation to high altitude in Himalayan and Andean populations. High Alt. Med. Biol. 2:211-25
123. Moore LG. 2001. Human genetic adaptation to high altitude. High Alt. Med. Biol. 2:257-79
124. Rupert JL, Hochachka PW. 2001. The evidence for hereditary factors contributing to high altitude adaptation in Andean natives: a review. High Alt. Med. Biol. 2:235-56
125. 2 saturation of arterial hemoglobin in Tibetan Highlanders. Am. J. Phys. Anthropol. 95:271-76
126. Beall CM, Strohl KP, Blangero J, Williams-Blangero S, Decker MJ, et al. 1997. Quantitative genetic analysis of arterial oxygen saturation in Tibetan Highlanders. Hum. Biol. 69:597-604
127. Hochachka PW, Rupert JL, Monge C. 1999. Adaptation and conservation of physiological systems in the evolution of human hypoxia tolerance. Comp. Biochem. Physiol. A 124:1-17
128. O'Brien SJ, Menotti-Raymond M, Murphy WJ, Nash WG, Wienberg J, et al. 1999. The promise of comparative genomics in mammals. Science 286:458-81
129. Enard W, Khaitovich P, Klose J, Zollner S, Heissig F, et al. 2002. Intra- and interspecific variation in primate gene expression patterns. Science 296:340-43
130. Szewczak JM. 1997. Matching gas exchange in the bat from flight to torpor. Am. Zool. 37:92-100
131. Boggs DF. 1995. Hypoxic ventilatory control and hemoglobin oxygen affinity. In Hypoxia and the Brain, ed. JR Sutton, CS Houston, G Coates, pp. 69-86. Burlington, VT: Queen City Printers
132. Gilbert DL. 1996. Evolutionary aspects of atmospheric oxygen and organisms. In Handbook of Physiology Section 4: Environmental Physiology, ed. MJ Fregly, CM Blatteis, pp. 1059-94. New York: Oxford Univ. Press
133. Graham JB, Dudley R, Aguilar NM, Gans C. 1995. Implications of the late Palaeozoic oxygen pulse for physiology and evolution. Nature 375:117-20
134. Kasting JF. 2001. The rise of atmospheric oxygen. Science 293:819-20
135. 2 evolution. Science 287:1630-33
136. Canfield DE, Habicht KS, Thamdrup B. 2000. The Archean sulfur cycle and the early history of atmospheric oxygen. Science 288:658-61
137. Dingle RV, McMillan IK, Majoran S, Bisset L. 2001. Palaeo- oceanographical implications of early-Middle Miocene subtropical ostracod faunas from the continental shelf of the SE Atlantic Ocean. Palaeogeogr. Palaeoclimatol. Palaeoecol. 173:43-60
138. Allmon WD. 2001. Nutrients, temperature, disturbance, and evolution: a model for the late Cenozoic marine record of the western Atlantic. Palaeogeogr. Palaeoclimatol. Palaeoecol. 166:9-26
139. Yemane K, Kelts K. 1996. Isotope geochemistry of Upper Permian early diagenetic calcite concretions: implications for Late Permian waters and surface temperatures in continental Gondwana. Palaeogeogr. Palaeoclimatol. Palaeoecol. 125:51-73
140. Platt JR. 1964. Strong inference. Science 146:347-53
141. Omholt SW. 2002. Book review of Foundations of Systems Biology: Bridging the Genotype-Phenotype Gap, ed. H Kitanoe, 2001. Science 295:2220
142. Kooyman GL. 1989. Diverse Divers: Physiology and Behavior. Berlin: Springer-Verlag. Vol. 23
143. Block BA, Dewar H, Blackwell SB, Williams TD, Prince ED, et al. 2001. Migratory movements, depth preferences, and thermal biology of Atlantic bluefin tuna. Science 293:1310-14
144. Guyton AC, Coleman TG, Granger HJ. 1972. Circulation: overall regulation. Annu. Rev. Physiol. 34:13-46