Abstract
Analysis of human responses to hypobaric hypoxia in different lineages (lowlanders, Andean natives, Himalayan natives, and East Africans) indicates ‘conservative’ and ‘adaptable’ physiological characters involved in human responses to hypoxia. Conservative characters, arising by common descent, dominant and indeed define human physiology, but in five hypoxia response systems analyzed, we also found evidence for ‘adaptable’ characters at all levels of organization in all three high altitude lineages. Since Andeans and Himalayans have not shared common ancestry with East Africans for most of our species history, we suggest that their similar hypoxia physiology may represent the ‘ancestral’ condition for humans - an interpretation consistent with recent evidence indicating that our species evolved under ‘colder, drier, and higher’ conditions in East Africa where the phenotype would be simultaneously advantageous for endurance performance and for high altitude hypoxia. It is presumed that the phenotype was retained in low capacity form in highlanders and in higher capacity form in most lowland lineages (where it would be recognized by most physiologists as an endurance performance phenotype). Interestingly, it is easier for modern molecular evolution theory to account for the origin of ‘adaptable’ characters through positive selection than for conserved traits. Many conserved physiological systems are composed of so many gene products that it seems difficult to account for their unchanging state (for unchanging structure and function of hundreds of proteins linked in sequence to form the physiological system) by simple models of stabilizing selection.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
Similar content being viewed by others
References
Acker H, Xue D (1995) Mechanism of oxygen sensing in the carotid body in comparison with other oxygen sensing cells. News Physiol. Sci. 10, 211–216
Alien PS, Matheson GO, Zhu G, Gheorgiu D, Dunlop RS, Falcomer T, Stanley C, Hochachka PW (1997) Simultaneous 3 I P Magnetic Resonance spectroscopy of the soleus and gastrocnemius in Sherpas during graded calf muscle exercise. Amer. J. Physiol. 273, R999–R1007
Amu PMH, Simoneau JA, Boulay MR, Serresse CW, Theriault G, Bouchard C (1986) Skeletal muscle characteristics in sedentary Black and Caucasian males. J. Appl. Physiol. 61, 1758–1761
Antenzana AM, Richalet JP, Antenzana G, Spielvogel H, Kacini R.( 1992) Adrenergic system in high altitude residents. Intl. J. Sports Med. 13, S92–95
Antenzana AM, Richalet JP, Noriega I, Galarza M, Antenzana G (1995) Hormonal changes in normal and polycythemic high-altitude residents. J. Appl. Physiol. 79, 795–800
Brooks GA (1998) Mammalian fuel preferences during exercise. Comp. Biochem. Physiol., in press
Brooks GA, Fahey TD, and White TP (1996) Exercise Physiology-Human Biocnergetics and Its Applications. Mayfield Publ. Co., London pp 1–750.
Brooks GA, Butterfield GE, Wolfe RR, Groves BM, Mazzeo RS. Sutton JR, Wolfel EE, Reeves JT (1991) Increased dependence on blood glucose after acclimatization to 4,300 m. J. Appl. Physiol. 70, 919–927
Bunn HF, Poyton RO (1996) Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 76, 839–885
Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The History and Geography of Human Genes. Princeton Univ. Press, Princeton, NJ pp 1–535
Colice GL, Lawrason J, Munsef A, Bittle, P, Dietz J, Ramirez G (1993) Hormonal responses to exercise in high altitude natives and COPD patients. Aviation Space & Env. Med. 64, 512–516
Eyre-Walker, A. and Keightley, P.D. High genomic deleterious mutation rates in hominids. Nature 1999; 397, 344–347.
Fagard R, Biclen E, Amery A (1991) Heritability of aerobic power and anaerobic energy generation during exercise. J. Appl. Physiol. 70, 357–362
Favier R, Desplanches D, Hoppeler H, Caceres E, Grunenfelder A, Koubi H, Leuenberger M, Sempore B, Tuscher L, Spielvogel H (1996) Hormonal and metabolic adjustments during exercise in hypoxia and normoxia in highland natives. J. Appl. Physiol. 80, 632–637
Forsythe JS, Hang BH, Iyer NV, Agani F, Leung SW, Koos RD, Semenza GL (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cellular Biol. 16, 4604–4613
Golding GB (1994) In: Golding GB (ed), Non-Neutral Evolution — Theories and Molecular Data. Chapman and Hall, London, pp 126–138
Harik N, Harik SI, Kuo NT, Sakai K, Przybylski RJ, LaManna JC (1996) Time-course and reversibility of the hypoxia induced alterations in cerebral vascularity and cerebral capillary glucose transporter density. Brain Research 737, 335–338
Heath D, Williams DR (1981) Man at High Altitude. Churchill Livingstone, London pp 3–23
Henderson K, McCanse W, Urano T, and Gonzalez NC, FASEB J. 12, 5, 3701 (1998).
Hochachka PW (1992) Muscle enzymatic composition and metabolic regulation in high altitude adapted natives. Int. J. Sport Med. 13, S89–91
Hochachka PW (1994) Muscles as Molecular and Metabolic Machines. CRC Press, Boca Raton, Florida pp 1–158
Hochachka PW (1998) Mechanism and evolution of hypoxia-tolerance in humans. J. Exp. Biol. 201, 1243–1254.
Hochachka PW, and Mottishaw PD (1998) Evolution and adaptation of the diving response: Phocids and otariids. In: Pörtner HO, Playle R (eds) Cold Ocean Physiology, Cambridge University Press, Cambridge, UK 391–431.
Hochachka PW, Clark CM, Brown WD, Stanely C, Stone CK, Nickles RJ, Zhu G, Alien PS, Holden JE (1995) The brain at high altitude: Hypometabolism as a defense against chronic hypoxia? J. Cerebral Blood Flow and Metabolism, 14, 671–679
Hochachka PW, Clark CM, C.Monge C, Stanley C, Brown WD, Stone CK., Nickles RJ, Holden JE (1996) Sherpa brain glucose metabolism and defense adaptations against chronic hypoxia. J. Appl. Physiol., 81: 1355–1361
Hochachka PW, Clark CM, Holden JE, Stanley C, Ugurbil K, Menon RS (1996) 31P Magnetic Resonance Spectroscopy of the Sherpa Heart: A PCr/ATP Signature of Metabolic Defense Against Hypobaric Hypoxia. Proc. Natl. Acad. Sci., U.S.A. 93: 1215–1220
Hochachka PW, Gunga HC, Kirsch K (1998) Our ancestral physiological phenotype: An adaptation for hypoxia tolerance and for endurance performance? Proc. Natl. Acad. Sci. USA 95, 1915–1920
Hochachka PW, Somero GN (1984) Biochemical Adaptation. Princeton University Press, Princeton, pp 1–557
Hochachka PW, Stanley C, Matheson GO, McKenzie DC, Alien PS, Parkhousc WS (1991) Metabolic and work efficiencies during exercise in Andean natives. J. Appl. Physiol, 70: 1720–1730
Hochachka PW, Stanley C, McKenzie DC, Villena A, C Monge C (1992) Enzyme mechanisms for pyruvate-to-lactatc flux attentuation: A study of Sherpas, Quechuas, and hummingbirds Int. J. Sport Med. 13, S11–123
Hlolden JE, Stone CK, Brown WD, Nickles RJ, Stanley C, Clark CM, Hochachka PW (1995) Enhanced cardiac metabolism of plasma glucose in high altitude natives. Adaptations against chronic hypoxia J. Appl. Physiol., 79: 222–228
Jones S, Martin R, Pilbeam D, Editors (1995) Human Evolution. Cambridge Univ. Press, Cambridge, UK p 1–506
Kayser B, Hoppeler H, Classsen H, Cerretelli P (1991) Muscle structure and performance capacity of Himalayan Sherpas. J. Appl. Physiol. 70, 1938–1942
Kayser B, Hoppeler H, Desplanches D, Marconi C, Broers B, Cerretelli P (1996) Muscle ultrastructure and biochemistry in lowland Tibetans. J. Appl. Physiol. 80, 632–637
Kirkpatrick M (1997) Genes and adaptation: A pocket guide to the theory. In: Rose M R, Lauder GV (eds), Adaptation., Academic Press, San Diego, pp. 125–146
Ladoux A, Felin C (1993) Hypoxia is a strong inducer of vascular endothelial growth factor mRNA expression in the heartz Biochem. Biophys. Res. Commun. 195, 1005–1010
Lahiri S (1996) Peripheral chemoreceptors and their sensory neurons in chronic states of hypo-and hyperoxygenation. Handbook of Physiology 2 (4), 1183–1206
Lahiri S, Edelman NH, Cherniack NS, and Fishman AP (1969) Blunted hypoxic drive to ventilation in subjects with life-long hypoxemia. Fed. Proc. 28, 1289–1295
Levine RD, Stray-Gunderson J (1996) A practical approach to altitude training: Where to live and tram for optimal performance enhancement. J. Appl. Physiol. 13, S209–212
Mangum CP, Hochachka PW (1998) New directions in comparative physiology and biochemistry: Mechanisms, adaptations, and evolution. Physiol. Zool., 71, 471–484.
Matheson GO, Alien PS, Ellinger DC, Hanstock CC, Gheorghiu D, McKenzie DC, Stanley C, Parkhouse WS, Hochachka, PW (1991) Skeletal muscle metabolism and work capacity: a 3 I P-NMR study of Andean natives and lowlanders. J. Appl. Physiol., 70: 1963–1976
Matsubayashi K, Ozawa T, Nakashima M, Saito A, Fukuyamu H, Harada N, Kameyama M (1986) Cerebral blood flow and metabolism before and after staying at high altitude. J. Mountain Medicine 6, 51–57
Maxwell PH, Pugh CW, Ratcliffe PJ (1993) Inducible operation of the erythropoitin 3’ enhancer in multiple cell lines: evidence for a widespread oxygen sensing mechanism. Proc. Natl. Acad. Sci. USA 90, 2423–2427
Mazzeo RS, Bender PR, Brooks GA, Butterfield GE, Groves BM, Sutton JR, Wolfel EE, Reeves JT (1991) Arterial catecholamine responses during exercise with acute and chronic high-altitude exposure. Amer. J. Physiol. 261, E419–424
Moore LG, Curran-Everett L, Drama TS, Groves BM, McCullough RE, Sun SF, Sutton JR, Zamudio S, Zhuang JG (1992) Arc Tibetans better adapted? Intl. J. Sports Med. 13,S86–S88
Mottishaw PD, Thornton SK and Hochachka PW (1999). The diving response and its surprisingly evolutionary path in seals and sea lions. Amer. Zool., 39, 434–450.
Ogita HE, Nakaoka, T, Matsuoka R, Takao A, Kira Y (1994) Rapid induction of vascular endothelial growth factor expression by transient ischemia in rat heart. Amer. J. Physiol. 267, H1948–1954
Resink T, Buravkova L, Mirzapoyazova E, Kohler E, Erne P, Tkachuk V. (1996) Involvement of protein kinase C in hypoxia induced desensitization of the beta-adrenergic system in human endothelial cells. Biochem. Biophys. Res. Commun. 222, 753–758
Ridley M (1993) Evolution. Blackwell Scientific, Cambridge, MA, USA p141–183
Rosser BWC, Hochachka PW (1994) Metabolic capacity of muscle fibers from high-altitude natives. Europ. J. Appl. Physiol., 67: 513–517
Rumsey WL Abbot B, Bertelsen D, Mallamaci M, Hagan K, Nelson D, Erecinska M (1999) Adaptation to hypoxia alters energy metabolism in rat heart. Amer. J. Physiol., in press
Saltin B, Kim CK, Terrados N, Larsen H, Svedenhag J, Rolf CJ (1995) Morphology, enzyme activities, and buffer capacity in leg muscles of Kenyan and Scandinavian runners Scand. J. Med. Sci. Sports 5, 222–230
Saltin B, Larsen H, Torrados N, Bangsbo J, Bak T, Kim CK, Svedenhag J, Rolf CJ (1995) Aerobic exercise capacity at sea level and at altitude in Kenyan boys, junior and senior runners compared with Scandinavian runners. Scand. J. Med. Sci. Sports 5, 209–221
Samaja M, Mariani C, Prestini A, Cerretelli P (1997) Acid-base balance and 02 transport at high altitude. Acta Physiol. Scand. 159, 249–256
Strohl KP, Beall CM (1997) Ventilatory response to experimental hypoxia in adult male and female natives of the Tibetan and Andean pleateaus. In: Houston C. (ed) Women at Altitude. Queen City Printers, Burlington, VT pp 154–165
Terrados N (1992) Altitude training and muscular metabolism. Intl. J. Sports Med. 13, S206–209
Wang GL, Jian BH, Rue EA, Semenza G.L (1995) Hypoxia inducible factor 1 is a basic-helix-loop-helix PAS heterodimer regulated by cellular oxygen tension. Proc. Natl. Acad. Sci. USA 92, 5510–5514
Weir EK, Archer SL (1995) The mechanism of acute hypoxic pulmonary vasoconstriction: a tale of two channels. FASEB J. 9, 183–189
Wenger, RH, Gassman M (1997) Oxygen(es) and the hypoxia inducible factor 1. Biol. Chem. 378, 609–616
Winslow RM, C Mongr C (1987) Hypoxia, Polycythemia, and Chronic Mountain Sickness. Johns Hopkins Univ. Press, Baltimore, pp 1–255
Zamudio S, Droma T, Norkyel KY, Acharya G, Zamudio JA, Niermeyer SN, Moore LG (1993) Protection from intrauterine growth retardation in Tibetans at high altitude. Amer. J. Physical Anthropol. 91, 215–224 (1993).
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2002 Kluwer Academic Publishers
About this chapter
Cite this chapter
Hochachka, P.W., Carlos Monge, C. (2002). Evolution of Human Hypoxia Tolerance Physiology. In: Lahiri, S., Prabhakar, N.R., Forster, R.E. (eds) Oxygen Sensing. Advances in Experimental Medicine and Biology, vol 475. Springer, Boston, MA. https://doi.org/10.1007/0-306-46825-5_5
Download citation
DOI: https://doi.org/10.1007/0-306-46825-5_5
Publisher Name: Springer, Boston, MA
Print ISBN: 978-0-306-46367-9
Online ISBN: 978-0-306-46825-4
eBook Packages: Springer Book Archive