Hypoxia pp 133-151 | Cite as

Genetic and environmental adaptation in high altitude natives

Conceptual, methodological, and statistical concerns
  • Tom D. Brutsaert
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 502)


A great number of physiological and anthropological studies have investigated Andean and Himalayan populations native to high altitude (HA). A non-scientific survey of the extant literature reveals a relatively liberal tradition of inferring genetic (evolutionary) adaptation to HA in these groups, often based on limited evidence and/or based on study designs insufficient to fully address the issue. Rather than review the evidence for or against genetic adaptation, and in order to provide some perspective, this paper will review relevant conceptual, methodological, and statistical issues that are germane to the study of HA native human groups. In particular, focus will be on the limitations of the most common research approach which bases evolutionary inference on the comparison of phenotypic mean differences between highland and lowland native populations. The migrant study approach is discussed, as is a relatively new approach based on genetic admixture in hybrid populations.

Key words

natural selection developmental adaptation acclimatization hypoxia admixture migrant study 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Arnaud J, Gutierrez N, Tellez W, and Vergnes H. Haematology and erythrocyte metabolism in man at high altitude: an Aymara-Quechua comparison. American Journal of Physical Anthropology 67:279–284, 1985.PubMedCrossRefGoogle Scholar
  2. 2.
    Baker PT. Human adaptation to high altitude. Science 163:1149–56, 1969.PubMedCrossRefGoogle Scholar
  3. 3.
    Baynes RD, and Bothwell TH. Iron deficiency. Annu Rev Nutr 10:133–48, 1990.PubMedCrossRefGoogle Scholar
  4. 4.
    Beall CM. Tibetan and Andean contrasts in adaptation to high-altitude hypoxia. In: Oxygen Sensing: Molecule to Man, edited by Lahiri S.: Kluwer Academic/Plenum Publishers,2000, p. 63–74.Google Scholar
  5. 5.
    Beall CM, Almasy LA, Blangero J, Williams-Blangero S, Brittenham GM, Strohl KP, Decker MJ, Vargas E, Villena M, Soria R, Alarcon AM, and Gonzales C. Percent of oxygen saturation of arterial hemoglobin among Bolivian Aymara at 3,900–4,000 m. Am J Phys Anthropol 108:41–51,1999.PubMedCrossRefGoogle Scholar
  6. 6.
    Beall CM, Blangero J, Williams-Blangero S, and Goldstein MC. Major gene for percent of oxygen saturation of arterial hemoglobin in Tibetan highlanders. Am J Phys Anthropol 95:271–6, 1994.PubMedCrossRefGoogle Scholar
  7. 7.
    Beall CM, Strohl KP, Blangero J, Williams-Blangero S, Decker MJ, Brittenham GM, and Goldstein MC. Quantitative genetic analysis of arterial oxygen saturation in Tibetan highlanders. Hum Biol 69:597–604, 1997.PubMedGoogle Scholar
  8. 8.
    Beller U, Halle D, Catane R, Kaufman B, Hornreich G, and Levy-Lahad E. High frequency of BRCA1 and BRCA2 germline mutations in Ashkenazi Jewish ovarian cancer patients, regardless of family history. Gynecol Oncol 67:123–6, 1997.PubMedCrossRefGoogle Scholar
  9. 9.
    Bernado J. Maternal effects in animal ecology. American Zoologist 36:83–105, 1996.Google Scholar
  10. 10.
    Black CP, and Tenney SM. Oxygen transport during progressive hypoxia in high-altitude and sea- level waterfowl. Respir Physiol 39:217–39, 1980.PubMedCrossRefGoogle Scholar
  11. 11.
    Blangero J. Statistical genetic approaches to human adaptability. Hum Biol 65:941–66, 1993.PubMedGoogle Scholar
  12. 12.
    Blangero J, and Konigsberg LW. Multivariate segregation analysis using the mixed model. Genet Epidemiol 8:299–316, 1991.PubMedCrossRefGoogle Scholar
  13. 13.
    Blangero J, Williams JT, and Almasy L. Quantitative trait locus mapping using human pedigrees. Hum Biol 72:35–62, 2000.PubMedGoogle Scholar
  14. 14.
    Boning D, Maassen N, Jochum F, Steinacker J, Haider A, Thomas A, Schmidt W, Noe G, and Kubanek B. After-effects of a high altitude expedition on blood. Int J Sports Med 18:179–85, 1997.PubMedCrossRefGoogle Scholar
  15. 15.
    Boyce AJ, Haight JS, Rimmer DB, and Harrison GA. Respiratory function in Peruvian Quechua Indians. Ann Hum Biol 1:137–48, 1974.PubMedCrossRefGoogle Scholar
  16. 16.
    Brody JS, Lahiri S, Simpser M, Motoyama EK, and Velasquez T. Lung elasticity and airway dynamics in Peruvian natives to high altitude. J Appl Physiol 42:245–51., 1977.PubMedGoogle Scholar
  17. 17.
    Brutsaert TD, Araoz M, Soria R, Spielvogel H, and Haas JD. Higher arterial oxygen saturation during submaximal exercise in Bolivian Aymara compared to European sojourners and Europeans born and raised at high altitude. Am JPhys Anthropol 113:169–181, 2000.CrossRefGoogle Scholar
  18. 18.
    Brutsaert TD, Soria R, Caceres E, Spielvogel H, and Haas JD. Effect of developmental and ancestral high altitude exposure on chest morphology and pulmonary function in Andean and European/North American natives. American Journal of Human Biology 11:383–395,1999.PubMedCrossRefGoogle Scholar
  19. 19.
    Brutsaert TD, Spielvogel H, Soria R, Caceres E, Buzenet G, and Haas JD. Effect of developmental and ancestral high-altitude exposure on VO2 peak of Andean and European/North american natives. Am J Phys Anthropol 110:435–55, 1999.PubMedCrossRefGoogle Scholar
  20. 20.
    Cardich A. The origin of the Andean civilaztion. Antropologie 98:173–189, 1994.Google Scholar
  21. 21.
    Chakraborty R, Barton SA, Ferrell RE, and Schull WJ. Ethnicity determination by names among the Aymara of Chile and Bolivia. Hum Biol 61:159–77, 1989.PubMedGoogle Scholar
  22. 22.
    Chakraborty R, and Weiss KM. Admixture as a tool for finding linked genes and detecting that difference from allelic association between loci. Proc Natl Acad Sci U S A 85:9119–23., 1988.PubMedCrossRefGoogle Scholar
  23. 23.
    Chang KC. China. In: Chronologies in Old World Archaeology, edited by Ehrich RW. Chicago IL:University of Chicago Press, 1992.Google Scholar
  24. 24.
    Clausen J, Keck DD, and Hiesey WM. Experimental studies on the nature of species. III. Environmental responses of climatic races of Achillea. Baltimore: Lord Baltimore Press, 1948, p. 129.Google Scholar
  25. 25.
    Cook ND. Demographic Collapse, Indian Peru, 1520–1620. New York, NY, USA: Cambridge University Press, 1981.Google Scholar
  26. 26.
    Curran LS, Zhuang J, Droma T, and Moore LG. Superior exercise performance in lifelong Tibetan residents of 4,400 m compared with Tibetan residents of 3,658 m. Am J Phys Anthropol 105:21–31,1998.PubMedCrossRefGoogle Scholar
  27. 27.
    Curran LS, Zhuang J, Sun SF, and Moore LG. Ventilation and hypoxic ventilatory responsiveness in Chinese-Tibetan residents at 3,658 m. J Appl Physiol 83:2098–104, 1997.PubMedGoogle Scholar
  28. 28.
    de Meer K, Heymans HS, and Zijlstra WG. Physical adaptation of children to life at high altitude. Eur J Pediatr 154:263–72, 1995.PubMedCrossRefGoogle Scholar
  29. 29.
    DeGraff AC, Jr., Grover RF, Johnson RL, Jr., Hammond JW, Jr., and Miller JM. Diffusing capacity of the lung in Caucasians native to 3,100 m. J Appl Physiol 29:71–6, 1970.PubMedGoogle Scholar
  30. 30.
    Dempsey JA, Reddan WG, Birnbaum ML, Forster HV, Thoden JS, Grover RF, and Rankin J. Effects of acute through life-long hypoxic exposure on exercise pulmonary gas exchange. Respir Physiol 13:62–89, 1971.PubMedCrossRefGoogle Scholar
  31. 31.
    Droma T, McCullough RG, McCullough RE, Zhuang JG, Cymerman A, Sun SF, Sutton JR, and Moore LG. Increased vital and total lung capacities in Tibetan compared to Han residents of Lhasa (3,658 m). Am J Phys Anthropol 86:341–51, 1991.PubMedCrossRefGoogle Scholar
  32. 32.
    Dua GL, and Sen Gupta J. A study of physical work capacity of sea level residents on prolonged stay at high altitude and comparison with high altitude native residents. Indian J Physiol Pharmacol 24:15–24, 1980.PubMedGoogle Scholar
  33. 33.
    Elston RC, and Stewart J. A general model for the genetic analysis of pedigree data. Hum Hered 21:523–42, 1971.PubMedCrossRefGoogle Scholar
  34. 34.
    Falconer DS. Introduction to Quantitative Genetics. Essex: Longman House, 1981.Google Scholar
  35. 35.
    Favier R, Spielvogel H, Desplanches D, Ferretti G, Kayser B, and Hoppeler H. Maximal exercise performance in chronic hypoxia and acute normoxia in high-altitude natives. J Appl Physiol 78:1868–74, 1995.PubMedGoogle Scholar
  36. 36.
    Ferrell RE, Bertin T, Barton SA, Rothhammer F, and Schull WJ. The Multinational Andean Genetic and Health Program. IX. Gene frequencies and rare variants of 20 serum proteins and erythrocyte enzymes in the Aymara of Chile. Am J Hum Genet 32:92–102, 1980.PubMedGoogle Scholar
  37. 37.
    Ferrell RE, Bertin T, Young R, Barton SA, Murillo F, and Schull WJ. The Aymara of Western Bolivia. IV. Gene frequencies for eight blood groups and 19 protein and erythrocyte enzyme systems. Am J Hum Genet 30:539–49, 1978.PubMedGoogle Scholar
  38. 38.
    Frisancho AR. Developmental responses to high altitude hypoxia. Am J Phys Anthropol 32:401–7, 1970.PubMedCrossRefGoogle Scholar
  39. 39.
    Frisancho AR. Developmental adaptation to high altitude hypoxia. Int J Biometeorol 21:135–46, 1977.PubMedCrossRefGoogle Scholar
  40. 40.
    Frisancho AR, Frisancho HG, Albalak R, Villena M, Vargas E, and Soria R. Developmental, genetic and environmental components of lung volumes at high altitude. American Journal of Human Biology 9:191–203, 1997.CrossRefGoogle Scholar
  41. 41.
    Frisancho AR, Frisancho HG, Milotich M, Brutsaert T, Albalak R, Spielvogel H, Villena M, Vargas E, and Soria R. Developmental, genetic, and environmental components of aerobic capacity at high altitude. Am J Phys Anthropol 96:431–42, 1995.PubMedCrossRefGoogle Scholar
  42. 42.
    Frisancho AR, Martinez C, Velasquez T, Sanchez J, and Montoye H. Influence of developmental adaptation on aerobic capacity at high altitude. J Appl Physiol 34:176–80, 1973.PubMedGoogle Scholar
  43. 43.
    Garland TD, and Adolph SC. Physiological differentiation of vertebrate populations. Annu. Rev. Ecol. Syst. 22:193–228, 1991.CrossRefGoogle Scholar
  44. 44.
    Garland TJ, and Adolph SC. Why not do two-species comparative studies: limitations on inferring adaptation. Physiological Zoology 67:797–828, 1994.Google Scholar
  45. 45.
    Ge RL, Chen QH, Wang LH, Gen D, Yang P, Kubo K, Fujimoto K, Matsuzawa Y, Yoshimura K, Takeoka M, and et al. Higher exercise performance and lower VO2max in Tibetan than Han residents at 4,700 m altitude. J Appl Physiol 77:684–91, 1994.PubMedGoogle Scholar
  46. 46.
    Ge RL, He Lun GW, Chen QH, Li HL, Gen D, Kubo K, Matsuzawa Y, Fujimoto K, Yoshimura K, Takeoka M, and T. K. Comparisons of oxygen transport between Tibetan and Han residents at moderate altitude. Wilderness and Environmental medicine 6:391–400, 1995.CrossRefGoogle Scholar
  47. 47.
    Gledhill N, L.L. S, Frose AB, Wilkes DL, and Meyers EC. Acid base status with induced erythrocemia and its influence on arterial oxygenation during heavy exercise (Abstract). Med. Sci. Sports. Exer. 12:122, 1980.Google Scholar
  48. 48.
    Goelen G, Teugels E, Bonduelle M, Neyns B, and De Greve J. High frequency of BRCA1/2 germline mutations in 42 Belgian families with a small number of symptomatic subjects. J Med Genet 36:304–8, 1999.PubMedGoogle Scholar
  49. 49.
    Greksa LP. Effect of altitude on the stature, chest depth and forced vital capacity of low-to-high altitude migrant children of European ancestry. Hum Biol 60:23–32, 1988.PubMedGoogle Scholar
  50. 50.
    Greksa LP. Evidence for a genetic basis to the enhanced total lung capacity of Andean highlanders. Hum Biol 68:119–29, 1996.PubMedGoogle Scholar
  51. 51.
    Greksa LP, Haas JD, Leatherman TL, Thomas RB, and Spielvogel H. Work performance of high-altitude Aymara males. Ann Hum Biol 11:227–33, 1984.PubMedCrossRefGoogle Scholar
  52. 52.
    Greksa LP, Spielvogel H, and Caceres E. Total lung capacity in young highlanders of Aymara ancestry. Am J Phys Anthropol 94:477–86, 1994.PubMedCrossRefGoogle Scholar
  53. 53.
    Grover RF, Reeves JT, Grover EB, and Leathers JE. Muscular exercise in young men native to 3,100 m altitude. J Appl Physiol 22:555–64, 1967.PubMedGoogle Scholar
  54. 54.
    Groves BM, Droma T, Sutton JR, McCullough RG, McCullough RE, Zhuang J, Rapmund G, Sun S, Janes C, and Moore LG. Minimal hypoxic pulmonary hypertension in normal Tibetans at 3,658 m. J Appl Physiol 74:312–8, 1993.PubMedGoogle Scholar
  55. 55.
    Gulmezoglu M, de Onis M, and Villar J. Effectiveness of interventions to prevent or treat impaired fetal growth. Obstet Gynecol Surv 52:139–49, 1997.PubMedCrossRefGoogle Scholar
  56. 56.
    Haas JD. Maternal adaptation and fetal growth at high altitude in Bolivia. In: Social and Biological Predictors of Nutritional Status, Physical Growth, and Neurological Development., edited by Greene LS and Johnston FE. New York:Academic Press, 1980.Google Scholar
  57. 57.
    Haas JD, Frongillo EJ, Stepcik C, Beard J, and Hurtado L. Altitude, ethnic, and sex differences in birth weight and length in Bolivia. Human Biology 52:459–477, 1980.Google Scholar
  58. 58.
    Hall JM, Friedman L, Guenther C, Lee MK, Weber JL, Black DM, and King MC. Closing in on a breast cancer gene on chromosome 17q. Am J Hum Genet 50:1235–42, 1992.PubMedGoogle Scholar
  59. 59.
    Harrison GA. Human adaptability with reference to the IBP proposals for high altitude research. In: The Biology of Human Adaptability, edited by Baker PT and Weiner JS. Oxford:Clarendon Press, 1966, p. 509–520.Google Scholar
  60. 60.
    Harrison GA, Kuchemann CF, Moore MAS, Boyce AJ, Baju T, Mourant AE, Godber MJ, Glasgow BG, Kopec AC, and Tills D. The effects of altitudinal variation in Ethiopian populations. Philosophical Transactions of the Royal Society of London 256 Series B:147–182, 1969.CrossRefGoogle Scholar
  61. 61.
    Hochachka PW. Muscle enzymatic composition and metabolic regulation in high altitude adapted natives. Int J Sports Med 13 Suppl 1:S89–91, 1992.PubMedCrossRefGoogle Scholar
  62. 62.
    Hochachka PW. Mechanism and evolution of hypoxia-tolerance in humans. J Exp Biol 201:1243–54, 1998.PubMedGoogle Scholar
  63. 63.
    Hochachka PW, Clark CM, Brown WD, Stanley C, Stone CK, Nickles RJ, Zhu GG, Allen PS, and Holden JE. The brain at high altitude: hypometabolism as a defense against chronic hypoxia? J Cereb Blood Flow Metab 14:671–9, 1994.PubMedCrossRefGoogle Scholar
  64. 64.
    Hochachka PW, Clark CM, Holden JE, Stanley C, Ugurbil K, and Menon RS. 31P magnetic resonance spectroscopy of the Sherpa heart: a phosphocreatine/adenosine triphosphate signature of metabolic defense against hypobaric hypoxia. Proc Natl Acad Sci USA 93:1215–20, 1996.PubMedCrossRefGoogle Scholar
  65. 65.
    Hochachka PW, Clark CM, Monge C, Stanley C, Brown WD, Stone CK, Nickles RJ, and Holden JE. Sherpa brain glucose metabolism and defense adaptations against chronic hypoxia. J Appl Physiol 81:1355–61, 1996.PubMedGoogle Scholar
  66. 66.
    Hochachka PW, Gunga HC, and Kirsch K. Our ancestral physiological phenotype: an adaptation for hypoxia tolerance and for endurance performance? Proc Natl Acad Sci USA 95:1915–20, 1998.PubMedCrossRefGoogle Scholar
  67. 67.
    Hochachka PW, Stanley C, Matheson GO, McKenzie DC, Allen PS, and Parkhouse WS. Metabolic and work efficiencies during exercise in Andean natives. J Appl Physiol 70:1720–30, 1991.PubMedGoogle Scholar
  68. 68.
    Hoff C. Altitudinal variations in the physical growth and development of Peruvian Quechua children. Homo 24:87–99, 1974.Google Scholar
  69. 69.
    Holden JE, Stone CK, Clark CM, Brown WD, Nickles RJ, Stanley C, and Hochachka PW. Enhanced cardiac metabolism of plasma glucose in high-altitude natives: adaptation against chronic hypoxia. J Appl Physiol 79:222–8, 1995.PubMedGoogle Scholar
  70. 70.
    Hurtado A. Animals at high altitudes: resident man. In: Handbook of physiology, section 4, adaptation and environment, edited by D.B. Dill, E.F. Adolph, and C.G. Wiber. Washington, DC.:American Physiological Society, 1964, p. 843–60.Google Scholar
  71. 71.
    Johannssen W. Elemente der exakten erblichkeitslehre. Jena, Germany: Gustav Fisher, 1909.Google Scholar
  72. 72.
    Johnson RL, Jr., Cassidy SS, Grover RF, Schutte JE, and Epstein RH. Functional capacities of lungs and thorax in beagles after prolonged residence at 3,100 m. J Appl Physiol 59:1773–82,1985.PubMedGoogle Scholar
  73. 73.
    Jones RL, Man SF, Matheson GO, Parkhouse WS, Allen PS, McKenzie DC, and Hochachka PW. Overall and regional lung function in Andean natives after descent to low altitude. Respir Physiol 87:11–24, 1992.PubMedCrossRefGoogle Scholar
  74. 74.
    Kashiwazaki H, Dejima Y, Orias-Rivera J, and Coward WA. Energy expenditure determined by the doubly labeled water method in Bolivian Aymara living in a high altitude agropastoral community. Am J Clin Nutr 62:901–10, 1995.PubMedGoogle Scholar
  75. 75.
    Kayser B, Hoppeler H, Desplanches D, Marconi C, Broers B, and Cerretelli P. Muscle ultrastructure and biochemistry of lowland Tibetans. J Appl Physiol 81:419–25, 1996.PubMedGoogle Scholar
  76. 76.
    Kayser B, Marconi C, Amatya T, Basnyat B, Colombini A, Broers B, and Cerretelli P. The metabolic and ventilatory response to exercise in Tibetans born at low altitude. Respir Physiol 98:15–26, 1994.PubMedCrossRefGoogle Scholar
  77. 77.
    Kent P, O’Donoghue JM, O’Hanlon DM, Kerin MJ, Maher DJ, and Given HF. Linkage analysis and the susceptibility gene (BRCA-1) in familial breast cancer. Eur J Surg Oncol 21:240–1, 1995.PubMedCrossRefGoogle Scholar
  78. 78.
    Kollias J, Buskirk ER, Akers RF, Prokop EK, Baker PT, and Picon-Reategui E. Work capacity of long-time residents and newcomers to altitude. J Appl Physiol 24:792–9, 1968.PubMedGoogle Scholar
  79. 79.
    Kramer AA. Heritability estimates of thoracic skeletal dimensions for a high-altitude Peruvian population. In: Population studieson human adaptation and evolution in the Peruvian Andes, edited by Eckhardt RB and Melton TW. University Park, PA:Pennsylvania State University Press, 1992, p. 25–49.Google Scholar
  80. 80.
    Lalle P, De Latour M, Rio P, and Bignon YJ. Detection of allelic losses on 17q1-q21 chromosomal region in benign lesions and malignant tumors occurring in a familial context. Oncogene 9:437–42, 1994.PubMedGoogle Scholar
  81. 81.
    Lynch M, and Walsh B. Genetics and the analysis of quantitative traits. Sunderland, Massachusetts: Sinauer, 1998.Google Scholar
  82. 82.
    Matheson GO, Allen PS, Ellinger DC, Hanstock CC, Gheorghiu D, McKenzie DC, Stanley C, Parkhouse WS, and Hochachka PW. Skeletal muscle metabolism and work capacity: a 31P-NMR study of Andean natives and lowlanders. J Appl Physiol 70:1963–76, 1991.PubMedGoogle Scholar
  83. 83.
    Matson GA, Sutton HE, Swanson J, and Robinson A. Distribution of hereditary blood groups among Indians in South America. II. In Peru. Am JPhys Anthropol 24:325–49, 1966.CrossRefGoogle Scholar
  84. 84.
    Matson GA, Swanson J, and Robinson A. Distribution of hereditary blood groups among Indians in South America. 3. In Bolivia. Am J Phys Anthropol 25:13–33, 1966.PubMedCrossRefGoogle Scholar
  85. 85.
    Mazess RB. Exercise performance at high altitude in Peru. Fed Proc 28:1301–6, 1969.PubMedGoogle Scholar
  86. 86.
    Mazess RB. Exercise performance of Indian and white high altitude residents. Hum Biol 41:494–518, 1969.PubMedGoogle Scholar
  87. 87.
    Monge C, and Leon-Velarde F. Physiological Adaptation in High Altitude: Oxygen Transport in Mammals and Birds. Physiological Reviews 71:1135–1172, 1991.PubMedGoogle Scholar
  88. 88.
    Moore LG. Comparative aspects of high altitude adaptation in human populations. In: Oxygen Sensing: Molecule to Man, edited by al. S. Lahiri et al. Kluwer Academic/Plenum Publishers, 2000, p. 45–62.Google Scholar
  89. 89.
    Moore LG, Curran-Everett L, Droma TS, Groves BM, McCullough RE, McCullough RG, Sun SF, Sutton JR, Zamudio S, and Zhuang JG. Are Tibetans better adapted? Int J Sports Med 13 Suppl 1.S86–8, 1992.PubMedCrossRefGoogle Scholar
  90. 90.
    Moore LG, Niermeyer S, and Zamudio S. Human adaptation to high altitude: regional and life-cycle perspectives. Am J Phys Anthropol Suppl:25–64, 1998.CrossRefGoogle Scholar
  91. 91.
    Moore LG, and Regensteiner JG. Adaptation to High Altitude. Annu. Rev. Anthrop. 12:285–304, 1983.CrossRefGoogle Scholar
  92. 92.
    Moore LG, Zamudio S, Curran-Everett L, Torroni A, Jorde LB, Shohet RV, Drolkar T, and Drolkar T. Genetic Adaptation to High Altitude. In: Sports and Exercise Medicine, edited by Wood SC and Roach RC. New York:Dekker, 1994, p. 225–262.Google Scholar
  93. 93.
    Maternal Effects as Adaptations. Mousseau TA, and Fox CW, eds. New York:Oxford University Press, 1998,Google Scholar
  94. 94.
    Mueller WH, Chakraborty R, Barton SA, Rothhammer F, and Schull WJ. Genes and epidemiology in anthropological adaptation studies: familial correlations in lung function in populations residing different altitude in Chile. Med. Anthropol. 4:367–384, 1980.CrossRefGoogle Scholar
  95. 95.
    Mueller WH, Yen F, Rothhammer F, and Schull WJ. A multinational Andean genetic and health program: VI. Physiological measurements of lung function in an hypoxic environment. Hum Biol 50:489–513, 1978.PubMedGoogle Scholar
  96. 96.
    Niermeyer S, Yang P, Shanmina, Drolkar, Zhuang J, and Moore LG. Arterial oxygen saturation in Tibetan and Han infants born in Lhasa, Tibet. N Engl J Med 333:1248–52, 1995.PubMedCrossRefGoogle Scholar
  97. 97.
    Niu W, Wu Y, Li B, Chen N, and Song S. Effects of long-term acclimatization in lowlanders migrating to high altitude: comparison with high altitude residents. Eur J Appl Physiol 71:543–8, 1995.CrossRefGoogle Scholar
  98. 98.
    Paz-Zamora M, Coudert J, Ergueta C, Vargas E, and Gutierrez N. Respiratory and cardiocirculatory responses of acclimatization of high altitude natives (La Paz, 3500m) to tropical lowland (Santa Cruz, 420m). In: Topics in Environmental Physiology and Medicine: High Altitude Physiology and Medicine, edited by Brendel W and Zink RA. New York:Springer-Verlag, 1982, p. 21–27.CrossRefGoogle Scholar
  99. 99.
    Pei SX, Chen XJ, Si Ren BZ, Liu YH, Cheng XS, Harris EM, Anand IS, and Harris PC. Chronic mountain sickness in Tibet. Q J Med 71:555–74, 1989.PubMedGoogle Scholar
  100. 100.
    Polgar G, and Weng TR. The functional development of the respiratory system from the period of gestation to adulthood. Am Rev Respir Dis 120:625–95., 1979.PubMedGoogle Scholar
  101. 101.
    Ramakrishnan U, Martorell R, Schroeder DG, and Flores R. Role of intergenerational effects on linear growth. J Nutr 129:544S–549S, 1999.PubMedGoogle Scholar
  102. 102.
    Ramirez G, Bittle PA, Rosen R, Rabb H, and Pineda D. High altitude living: genetic and environmental adaptation. Aviat Space Environ Med 70:73–81, 1999.PubMedGoogle Scholar
  103. 103.
    Relethford JH, and Lees FC. The use of quantitative traits in the study of human population structure. Yearbook of physical anthropology 25:113–132, 1982.CrossRefGoogle Scholar
  104. 104.
    Rogers J, Mahaney MC, Almasy L, Comuzzie AG, and Blangero J. Quantitative trait linkage mapping in anthropology. Am J Phys Anthropol 110:127–151, 1999.CrossRefGoogle Scholar
  105. 105.
    Rupert JL, Devine DV, Monsalve MV, and Hochachka PW. Angiotensin-Converting enzyme (ACE) alleles in the Quechua, a high altitude South American native population. Ann Hum Biol 26:375–80, 1999.PubMedCrossRefGoogle Scholar
  106. 106.
    Rupert JL, Devine DV, Monsalve MV, and Hochachka PW. Beta-fibrinogen allele frequencies in Peruvian Quechua, a high-altitude native population. Am J Phys Anthropol 109:181–6, 1999.PubMedCrossRefGoogle Scholar
  107. 107.
    Saltin B, and Gollnick PD. Skeletal muscle adaptability: significance for metabolism and performance. In: Handbook of Physiology. Skeletal muscle, Bethesda, MD.:Am. Physiol. Soc., 1983, p. 555–631.Google Scholar
  108. 108.
    Santolaya RB, Lahiri S, Alfaro RT, and Schoene RB. Respiratory adaptation in the highest inhabitants and highest Sherpa mountaineers. Respir Physiol 77:253–62, 1989.PubMedCrossRefGoogle Scholar
  109. 109.
    Schoene RB RR, Lahiri S, Peters RM, Hackett PH, and Santolaya R. Increased diffusion capacity maintains arterial saturation during exercise in the Quechua Indians of the Chilean Altiplano. Am J Hum Bio 2:663–668, 1990.CrossRefGoogle Scholar
  110. 110.
    Sun SF, Droma TS, Zhang JG, Tao JX, Huang SY, McCullough RG, McCullough RE, Reeves CS, Reeves JT, and Moore LG. Greater maximal O2 uptakes and vital capacities in Tibetan than Han residents of Lhasa. Respir Physiol 79:151–61, 1990.PubMedCrossRefGoogle Scholar
  111. 111.
    Vogel JA, Hartley LH, and Cruz JC. Cardiac output during exercise in altitude natives at sea level and high altitude. J Appl Physiol 36:173–6., 1974.PubMedGoogle Scholar
  112. 112.
    Way AB. Exercise capacity of high altitude peruvian Quechua Indians migrant to low altitude. Hum Biol 48:175–91, 1976.PubMedGoogle Scholar
  113. 113.
    West JB. Respiratory and circulatory control at high altitudes. J Exp Biol 100:147–57, 1982.PubMedGoogle Scholar
  114. 114.
    Williams JH, Powers SK, and Stuart MK. Hemoglobin desaturation in highly trained athletes during heavy exercise. Med Sci Sports Exerc 18:168–73, 1986.PubMedGoogle Scholar
  115. 115.
    Williams RC, Long JC, Hanson RL, Sievers ML, and Knowler WC. Individual estimates of European genetic admixture associated with lower body-mass index, plasma glucose, and prevalence of type 2 diabetes in Pima Indians. Am J Hum Genet 66:527–38., 2000.PubMedCrossRefGoogle Scholar
  116. 116.
    Winslow RM, Chapman KW, Gibson CC, Samaja M, Monge CC, Goldwasser E, Sherpa M, Blume FD, and Santolaya R. Different hematologic responses to hypoxia in Sherpas and Quechua Indians. J Appl Physiol 66:1561–9, 1989.PubMedGoogle Scholar
  117. 117.
    Zamudio S, Droma T, Norkyel KY, Acharya G, Zamudio JA, Niermeyer SN, and Moore LG. Protection from intrauterine growth retardation in Tibetans at high altitude. Am J Phys Anthropol 91:215–24, 1993.PubMedCrossRefGoogle Scholar
  118. 118.
    Zhimin A. Paleoliths and microliths from Shenja and Shuanghu, Northern Tibet. Curr. Anthropol 23:493–499, 1982.CrossRefGoogle Scholar
  119. 119.
    Zhuang J, Droma T, Sun S, Janes C, McCullough RE, McCullough RG, Cymerman A, Huang SY, Reeves JT, and Moore LG. Hypoxic ventilatory responsiveness in Tibetan compared with Han residents of 3,658 m. J Appl Physiol 74:303–11, 1993.PubMedGoogle Scholar
  120. 120.
    Zhuang J, Droma T, Sutton JR, Groves BM, McCullough RE, McCullough RG, Sun S, and Moore LG. Smaller alveolar-arterial O2 gradients in Tibetan than Han residents of Lhasa (3658 m). Respir Physiol 103:75–82, 1996.PubMedCrossRefGoogle Scholar
  121. 121.
    Zweemer RP, Shaw PA, Verheijen RM, Ryan A, Berchuck A, Ponder BA, Risch H, McLaughlin JR, Narod SA, Menko FH, Kenemans P, and Jacobs IJ. Accumulation of p53 protein is frequent in ovarian cancers associated with BRCA1 and BRCA2 germline mutations. J Clin Pathol 52:372–5, 1999.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2001

Authors and Affiliations

  • Tom D. Brutsaert
    • 1
  1. 1.Department of AnthropologyThe State University of New YorkAlbanyUSA

Personalised recommendations