The Andean adaptive toolkit to counteract high altitude maladaptation: Genome-wide and phenotypic analysis of the Collas

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Eichstaedt, Christina A ^a   Antão, Tiago ^b   Pagani, Luca ^a,c   Cardona, Alexia ^a   Kivisild, Toomas ^a   Mormina, Maru ^a,d  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d UNIVERSITY OF EAST ANGLIA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA; VASCULOTROPIN B; OXYGEN;

ADULT; ALTITUDE ACCLIMATIZATION; ALTITUDE DISEASE; ARGENTINA; ARTICLE; BODY MASS; BODY WEIGHT; BRAIN BLOOD FLOW; BREATHING PATTERN; ELTD1 GENE; GENE; GENE FLOW; GENE FREQUENCY; GENETIC VARIABILITY; HEART OUTPUT; HEART RATE; HEMATOCRIT; HOMOZYGOSITY; HUMAN; HUMAN EXPERIMENT; NORMAL HUMAN; OXYGEN SATURATION; SINGLE NUCLEOTIDE POLYMORPHISM; SYSTOLIC BLOOD PRESSURE; VEGFB GENE; ACCLIMATIZATION; ADAPTATION; ALTITUDE; ANOXIA; ECOSYSTEM; EVOLUTION; GENETIC ASSOCIATION; GENETICS; GENOTYPE; METABOLISM; POPULATION GENETICS; PROCEDURES; SOUTH AMERICA;

ACCLIMATIZATION; ADAPTATION, PHYSIOLOGICAL; ALTITUDE; ANOXIA; BIOLOGICAL EVOLUTION; ECOSYSTEM; GENETICS, POPULATION; GENOME-WIDE ASSOCIATION STUDY; GENOTYPE; HUMANS; OXYGEN; POLYMORPHISM, SINGLE NUCLEOTIDE; SOUTH AMERICA;

EID: 84899811310     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093314     Document Type: Article

References (106)

1. Hawks J, Wang ET, Cochran GM, Harpending HC, Moyzis RK (2007) Recent acceleration of human adaptive evolution. Proc Natl Acad Sci U S A 104: 20753-20758.
2. West JB, Schoene RB, Milledge JS, Ward MP (2007) High altitude medicine and physiology. London: Hodder Arnold. xii, 484 p. p.
3. Center for International Earth Science Information Network (CIESIN)/Columbia University (2012) National Aggregates of Geospatial Data: Population, Landscape and Climate Estimates Version 3 (PLACE III). Palisades, New York: NASA Socioeconomic Data and Applications Center.
4. Beall CM (2006) Andean, Tibetan, and Ethiopian patterns of adaptation to high-altitude hypoxia. Annual Meeting of the Society for Integrative and Comparative Biology. San Diego, California: Integrative and Comparative Biology. pp. 18-24.
5. Aldenderfer M (2003) Moving Up in the World: Archaeologists seek to understand how and when people came to occupy the Andean and Tibetan plateaus. American Scientist 91: 542-549.
6. Levett DZ, Radford EJ, Menassa DA, Graber EF, Morash AJ, et al. (2012) Acclimatization of skeletal muscle mitochondria to high-altitude hypoxia during an ascent of Everest. FASEB J 26: 1431-1441.
7. Beall CM, Strohl KP, Blangero J, Williams-Blangero S, Almasy LA, et al. (1997) Ventilation and hypoxic ventilatory response of Tibetan and Aymara high altitude natives. Am J Phys Anthropol 104: 427-447. (Pubitemid 28034619)
8. Brutsaert TD, Araoz M, Soria R, Spielvogel H, Haas JD (2000) Higher arterial oxygen saturation during submaximal exercise in Bolivian Aymara compared to European sojourners and Europeans born and raised at high altitude. Am J Phys Anthropol 113: 169-181. (Pubitemid 33051132)
9. Gaya-Vidal M, Moral P, Saenz-Ruales N, Gerbault P, Tonasso L, et al. (2011) mtDNA and Y-chromosome diversity in Aymaras and Quechuas from Bolivia: different stories and special genetic traits of the Andean Altiplano populations. Am J Phys Anthropol 145: 215-230.
10. Lundby C, Calbet JA, van Hall G, Saltin B, Sander M (2004) Pulmonary gas exchange at maximal exercise in Danish lowlanders during 8 wk of acclimatization to 4,100 m and in high-altitude Aymara natives. Am J Physiol Regul Integr Comp Physiol 287: R1202-1208. (Pubitemid 39391066)
11. Rupert JL, Hochachka PW (2001) Genetic approaches to understanding human adaptation to altitude in the Andes. J Exp Biol 204: 3151-3160. (Pubitemid 34861357)
12. Bigham AW, Kiyamu M, León-Velarde F, Parra EJ, Rivera-Ch M, et al. (2008) Angiotensin-converting enzyme genotype and arterial oxygen saturation at high altitude in Peruvian Quechua. High Alt Med Biol 9: 167-178. (Pubitemid 351913536)
13. Frisancho AR, Borkan GA, Klayman JE (1975) Pattern of growth of lowland and highland Peruvian Quechua of similar genetic composition. Hum Biol 47: 233-243.
14. Giussani DA, Phillips PS, Anstee S, Barker DJ (2001) Effects of altitude versus economic status on birth weight and body shape at birth. Pediatr Res 49: 490-494. (Pubitemid 32274961)
15. Bigham A, Bauchet M, Pinto D, Mao X, Akey JM, et al. (2010) Identifying signatures of natural selection in Tibetan and Andean populations using dense genome scan data. PLoS Genet 6: e1001116.
16. Bigham AW, Mao X, Mei R, Brutsaert T, Wilson MJ, et al. (2009) Identifying positive selection candidate loci for high-altitude adaptation in Andean populations. Hum Genomics 4: 79-90.
17. Zhou D, Udpa N, Ronen R, Stobdan T, Liang J, et al. (2013) Whole-Genome Sequencing Uncovers the Genetic Basis of Chronic Mountain Sickness in Andean Highlanders. Am J Hum Genet.
18. Virués-Ortega J, Garrido E, Javierre C, Kloezeman KC (2006) Human behaviour and development under high-altitude conditions. Dev Sci 9: 400-410. (Pubitemid 43855819)
19. Martin D, Windsor J (2008) From mountain to bedside: understanding the clinical relevance of human acclimatisation to high-altitude hypoxia. Postgrad Med J 84: 622-627; quiz 626.
20. Dorward DA, Thompson AA, Baillie JK, MacDougall M, Hirani N (2007) Change in plasma vascular endothelial growth factor during onset and recovery from acute mountain sickness. Respir Med 101: 587-594. (Pubitemid 46209926)
21. Aldashev AA, Kojonazarov BK, Amatov TA, Sooronbaev TM, Mirrakhimov MM, et al. (2005) Phosphodiesterase type 5 and high altitude pulmonary hypertension. Thorax 60: 683-687. (Pubitemid 41129068)
22. Beall CM (2007) Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci U S A 104 Suppl 1: 8655-8660.
23. Monge C, Whittembury J (1982) Chronic mountain sickness and the pathophysiology of hypoxemic polycythemia. In: Sutton JR, Houston CS, Jones NL, editors. Hypoxia: man at altitude. New York: Thieme-Stratton. pp. 51-56.
24. Villafuerte FC, Cardenas R, Monge CC (2004) Optimal hemoglobin concentration and high altitude: a theoretical approach for Andean men at rest. J Appl Physiol 96: 1581-1588. (Pubitemid 38579978)
25. Penaloza D, Arias-Stella J (2007) The heart and pulmonary circulation at high altitudes: healthy highlanders and chronic mountain sickness. Circulation 115: 1132-1146. (Pubitemid 46673174)
26. Heath D, Williams DR (1995) High-altitude medicine and pathology. Oxford: Oxford University Press. x,449p p.
27. Jansen GF, Basnyat B (2011) Brain blood flow in Andean and Himalayan high-altitude populations: evidence of different traits for the same environmental constraint. J Cereb Blood Flow Metab 31: 706-714.
28. Beall CM, Cavalleri GL, Deng L, Elston RC, Gao Y, et al. (2010) Natural selection on EPAS1 (HIF2a) associated with low hemoglobin concentration in Tibetan highlanders. Proc Natl Acad Sci U S A 107: 11459-11464.
29. Peng Y, Yang Z, Zhang H, Cui C, Qi X, et al. (2011) Genetic variations in Tibetan populations and high-altitude adaptation at the Himalayas. Mol Biol Evol 28: 1075-1081.
30. Simonson TS, Yang Y, Huff CD, Yun H, Qin G, et al. (2010) Genetic Evidence for High-Altitude Adaptation in Tibet. Science.
31. Wang B, Zhang YB, Zhang F, Lin H, Wang X, et al. (2011) On the origin of Tibetans and their genetic basis in adapting high-altitude environments. PLoS One 6: e17002.
32. Xu S, Li S, Yang Y, Tan J, Lou H, et al. (2011) A genome-wide search for signals of high-altitude adaptation in Tibetans. Mol Biol Evol 28: 1003-1011.
33. Yi X, Liang Y, Huerta-Sanchez E, Jin X, Cuo ZX, et al. (2010) Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329: 75-78.
34. Bauer M, Glenn T, Rasgon N, Marsh W, Sagduyu K, et al. (2010) Association between age of onset and mood in bipolar disorder: comparison of subgroups identified by cluster analysis and clinical observation. J Psychiatr Res 44: 1170-1175.
35. Simonson TS, Yang Y, Huff CD, Yun H, Qin G, et al. (2010) Genetic evidence for high-altitude adaptation in Tibet. Science 329: 72-75.
36. Pagani L, Ayub Q, Macarthur DG, Xue Y, Baillie JK, et al. (2012) High altitude adaptation in Daghestani populations from the Caucasus. Hum Genet 131: 423-433.
37. Bigham AW, Wilson MJ, Julian CG, Kiyamu M, Vargas E, et al. (2013) Andean and Tibetan patterns of adaptation to high altitude. Am J Hum Biol.
38. Beall CM, Laskowski D, Strohl KP, Soria R, Villena M, et al. (2001) Pulmonary nitric oxide in mountain dwellers. Nature 414: 411-412. (Pubitemid 34173716)
39. Xing G, Qualls C, Huicho L, Rivera-Ch M, Stobdan T, et al. (2008) Adaptation and mal-adaptation to ambient hypoxia; Andean, Ethiopian and Himalayan patterns. PLoS One 3: e2342.
40. Igwe EI, Essler S, Al-Furoukh N, Dehne N, Brune B (2009) Hypoxic transcription gene profiles under the modulation of nitric oxide in nuclear run on-microarray and proteomics. BMC Genomics 10: 408.
41. Thornton KR, Jensen JD (2007) Controlling the false-positive rate in multilocus genome scans for selection. Genetics 175: 737-750. (Pubitemid 46798272)
42. Frank S (2008) Pueblos Originarios de América. Buenos Aires: Ediciones de Sol S.R.L.
43. Rothhammer F, Silva C (1989) Peopling of Andean South America. Am J Phys Anthropol 78: 403-410. (Pubitemid 19076960)
44. Acreche N, Albeza M, Caruso GB, Broglia VG, Acosta R (2004) Diversidad biológica humana en la provincia de Salta (Human biological diversity in Salta) Cuadernos FHYCS-UNJu 22: 171-194.
45. Rothhammer F, Santoro C (2001) Cultural development in the Azapa Valley in the far north of Chile, and its connection with population displacement in the highlands. Latin American Antiquity 12: 59-66.
46. Braunstein J, Miller E (2001) Ethnohistorical introduction. In: Miller E, editor. Peoples of the Gran Chaco. Westport, CT: Greenwood Publishing Group.
47. Demarchi DA, Mitchell RJ (2004) Genetic structure and gene flow in Gran Chaco populations of Argentina: evidence from Y-chromosome markers. Hum Biol 76: 413-429. (Pubitemid 39274412)
48. Cabana GS, Merriwether DA, Hunley K, Demarchi DA (2006) Is the genetic structure of Gran Chaco populations unique? Interregional perspectives on native South American mitochondrial DNA variation. Am J Phys Anthropol 131: 108-119. (Pubitemid 44267107)
49. Sala A, Penacino G, Corach D (1998) Comparison of allele frequencies of eight STR loci from Argentinian Amerindian and European populations. Hum Biol 70: 937-947. (Pubitemid 28514479)
50. Sevini F, Yao DY, Lomartire L, Barbieri A, Vianello D, et al. (2013) Analysis of population substructure in two sympatric populations of Gran Chaco, Argentina. PLoS One 8: e64054.
51. U.S. Department of Agriculture (2008) USDA Food Search. Release 21 ed. Beltsville, Maryland: Agricultural Research Service.
52. Quinque D, Kittler R, Kayser M, Stoneking M, Nasidze I (2006) Evaluation of saliva as a source of human DNA for population and association studies. Anal Biochem 353: 272-277. (Pubitemid 43775441)
53. Delaneau O, Marchini J, Zagury JF (2011) A linear complexity phasing method for thousands of genomes. Nat Methods 9: 179-181.
54. Hill C, Soares P, Mormina M, Macaulay V, Clarke D, et al. (2007) A mitochondrial stratigraphy for island Southeast Asia. Am J Hum Genet 80: 29-43. (Pubitemid 46047648)
55. Sykes B, Leiboff A, Low-Beer J, Tetzner S, Richards M (1995) The origins of the Polynesians: an interpretation from mitochondrial lineage analysis. Am J Hum Genet 57: 1463-1475.
56. Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105: 437-460.
57. Nei M (1987) Molecular evolutionary genetics. New York: Columbia University Press.x,512 p.
58. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47-50.
59. Corach D, Lao O, Bobillo C, van Der Gaag K, Zuniga S, et al. (2010) Inferring continental ancestry of Argentineans from autosomal, Y-chromosomal and mitochondrial DNA. Ann Hum Genet 74: 65-76.
60. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, et al. (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81: 559-575. (Pubitemid 47330214)
61. International HapMap-Consortium (2003) The International HapMap Project. Nature 426: 789-796.
62. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, et al. (2008) Worldwide human relationships inferred from genome-wide patterns of variation. Science 319: 1100-1104. (Pubitemid 351300793)
63. Mao X, Bigham AW, Mei R, Gutierrez G, Weiss KM, et al. (2007) A genomewide admixture mapping panel for Hispanic/Latino populations. Am J Hum Genet 80: 1171-1178. (Pubitemid 47579352)
64. Reich D, Patterson N, Campbell D, Tandon A, Mazieres S, et al. (2012) Reconstructing Native American population history. Nature 488: 370-374.
65. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19: 1655-1664.
66. Alexander DH, Lange K (2011) Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinformatics 12: 246.
67. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2: e190.
68. Pickrell JK, Pritchard JK (2012) Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet 8: e1002967.
69. Reich D, Thangaraj K, Patterson N, Price AL, Singh L (2009) Reconstructing Indian population history. Nature 461: 489-494.
70. Levett DZ, Martin DS, Wilson MH, Mitchell K, Dhillon S, et al. (2010) Design and conduct of Caudwell Xtreme Everest: an observational cohort study of variation in human adaptation to progressive environmental hypoxia. BMC Med Res Methodol 10: 98.
71. Frisancho AR (2008) Anthropometric standards: an interactive nutritional reference of body size and body composition for children and adults. Ann Arbor: University of Michigan Press. viii, 335 p. p.
72. Cameron N (1981) Anthropometry. In: Weiner JS, Lourie JA, editors. Practical human biology. London: Academic Press. pp. 27-52.
73. de Simone G, Roman MJ, Koren MJ, Mensah GA, Ganau A, et al. (1999) Stroke volume/pulse pressure ratio and cardiovascular risk in arterial hypertension. Hypertension 33: 800-805. (Pubitemid 29140437)
74. Pickrell JK, Coop G, Novembre J, Kudaravalli S, Li JZ, et al. (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res 19: 826-837.
75. International HapMap Consortium, Frazer KA, Ballinger DG, Cox DR, Hinds DA, et al. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851-861.
76. Flicek P, Amode MR, Barrell D, Beal K, Brent S, et al. (2012) Ensembl 2012. Nucleic Acids Res 40: D84-90.
77. Raymond M, Rousset F (1995) GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. J Heredity: 248-249.
78. Rousset F (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour: 103-106.
79. Shriver MD, Kennedy GC, Parra EJ, Lawson HA, Sonpar V, et al. (2004) The genomic distribution of population substructure in four populations using 8,525 autosomal SNPs. Hum Genomics 1: 274-286.
80. Hosack DA, Dennis G, Jr., Sherman BT, Lane HC, Lempicki RA (2003) Identifying biological themes within lists of genes with EASE. Genome Biol 4: R70.
81. Dennis G, Jr., Sherman BT, Hosack DA, Yang J, Gao W, et al. (2003) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3.
82. Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
83. Sabeti PC, Reich DE, Higgins JM, Levine HZ, Richter DJ, et al. (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419: 832-837. (Pubitemid 35238568)
84. Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4: e72.
85. Langergraber KE, Prufer K, Rowney C, Boesch C, Crockford C, et al. (2012) Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proc Natl Acad Sci U S A 109: 15716-15721.
86. Brutsaert TD, Soria R, Caceres E, Spielvogel H, Haas JD (1999) Effect of developmental and ancestral high altitude exposure on chest morphology and pulmonary function in Andean and European/North American natives. Am J Hum Biol 11: 383-395. (Pubitemid 129726308)
87. Tarazona-Santos E, Lavine M, Pastor S, Fiori G, Pettener D (2000) Hematological and pulmonary responses to high altitude in Quechuas: a multivariate approach. Am J Phys Anthropol 111: 165-176. (Pubitemid 30080395)
88. Sabeti PC, Varilly P, Fry B, Lohmueller J, Hostetter E, et al. (2007) Genomewide detection and characterization of positive selection in human populations. Nature 449: 913-918. (Pubitemid 47598625)
89. Nechiporuk T, Urness LD, Keating MT (2001) ETL, a novel seven-transmembrane receptor that is developmentally regulated in the heart. J Biol Chem 276: 4150-4157.
90. + involving hypoxia-inducible factor-1α and the von Hippel-Lindau protein. J Physiol 571: 349-359.
91. Morikawa T, Kajimura M, Nakamura T, Hishiki T, Nakanishi T, et al. (2012) Hypoxic regulation of the cerebral microcirculation is mediated by a carbon monoxide-sensitive hydrogen sulfide pathway. Proc Natl Acad Sci U S A 109: 1293-1298.
92. Alkorta-Aranburu G, Beall CM, Witonsky DB, Gebremedhin A, Pritchard JK, et al. (2012) The genetic architecture of adaptations to high altitude in Ethiopia. PLoS Genet 8: e1003110.
93. Scheinfeldt LB, Soi S, Thompson S, Ranciaro A, Meskel DW, et al. (2012) Genetic adaptation to high altitude in the Ethiopian highlands. Genome Biol 13: R1.
94. Huerta-Sanchez E, Degiorgio M, Pagani L, Tarekegn A, Ekong R, et al. (2013) Genetic signatures reveal high-altitude adaptation in a set of Ethiopian populations. Mol Biol Evol 30: 1877-1888.
95. Fagundes NJ, Kanitz R, Eckert R, Valls AC, Bogo MR, et al. (2008) Mitochondrial population genomics supports a single pre-Clovis origin with a coastal route for the peopling of the Americas. Am J Hum Genet 82: 583-592.
96. Fransen M, Nordgren M, Wang B, Apanasets O (2012) Role of peroxisomes in ROS/RNS-metabolism: Implications for human disease. Biochim Biophys Acta 1822: 1363-1373.
97. Li X, Tjwa M, Van Hove I, Enholm B, Neven E, et al. (2008) Reevaluation of the role of VEGF-B suggests a restricted role in the revascularization of the ischemic myocardium. Arterioscler Thromb Vasc Biol 28: 1614-1620.
98. Egan JR, Butler TL, Cole AD, Aharonyan A, Baines D, et al. (2008) Myocardial ischemia is more important than the effects of cardiopulmonary bypass on myocardial water handling and postoperative dysfunction: a pediatric animal model. J Thorac Cardiovasc Surg 136: 1265-1273.
99. Heggarty P, Beresford-Jones D (2010) Agriculture and Language Dispersals: Limitations, Refinements, and an Andean Exception? Curr Anthropol 51.
100. Nordstrom DK (2002) Public health. Worldwide occurrences of arsenic in ground water. Science 296: 2143-2145.
101. Moore LG (2001) Human genetic adaptation to high altitude. High Alt Med Biol 2: 257-279.
102. Arad M, Seidman CE, Seidman JG (2007) AMP-activated protein kinase in the heart: role during health and disease. Circ Res 100: 474-488. (Pubitemid 46673257)
103. Clark AG, Hubisz MJ, Bustamante CD, Williamson SH, Nielsen R (2005) Ascertainment bias in studies of human genome-wide polymorphism. Genome Res 15: 1496-1502. (Pubitemid 41545003)
104. Pritchard JK, Pickrell JK, Coop G (2010) The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol 20: R208-215.
105. Albeza MV, Acreche NE, Caruso GB (2002) Biodemografía en poblaciones de la Puna (Chañarcito, Santa Rosa de los Pastos Grandes y Olacapato) Salta, Argentina. (Biodemography of Puna populations (Chañarcito, Santa Rosa de los Pastos Grandes and Olacapato) Salta, Argentina). Chungara, Revista de Antropología Chilena 34: 119-126.
106. Bowcock AM, Kidd JR, Mountain JL, Hebert JM, Carotenuto L, et al. (1991) Drift, admixture, and selection in human evolution: a study with DNA polymorphisms. Proc Natl Acad Sci U S A 88: 839-843. (Pubitemid 21916119)