Genome-wide analysis of cold adaptation in indigenous Siberian populations

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Cardona, Alexia ^a   Pagani, Luca ^a,b   Antao, Tiago ^c   Lawson, Daniel J ^d   Eichstaedt, Christina A ^a   Yngvadottir, Bryndis ^a   Shwe, Ma Than Than ^e   Wee, Joseph ^e   Romero, Irene Gallego ^f   Raj, Srilakshmi ^g   Metspalu, Mait ^h,i   Villems, Richard ^h,i   Willerslev, Eske ^j   Tyler Smith, Chris ^b   Malyarchuk, Boris A ^k   Derenko, Miroslava V ^k   Kivisild, Toomas ^a,i  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

^e DIVISION OF MEDICAL ONCOLOGY   (Singapore)

^f UNIVERSITY OF CHICAGO   (United States)

^g Department of Obstetrics Gynecology   (United States)

^h UNIVERSITY OF TARTU   (Estonia)

ⁱ UNIVERSITY OF TARTU   (Estonia)

^j UNIVERSITY OF COPENHAGEN   (Denmark)

^k INSTITUTE OF BIOLOGICAL PROBLEMS OF THE NORTH   (Russian Federation)

more..

Author keywords

[No Author keywords available]

Indexed keywords

LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 5;

ARTICLE; CHROMOSOME STRUCTURE; COLD ACCLIMATIZATION; CONTROLLED STUDY; CPT1A GENE; ENERGY METABOLISM; GENE; GENE FREQUENCY; GENE IDENTIFICATION; GENETIC SELECTION; GENOME ANALYSIS; GENOTYPE; HAPLOTYPE; HOMOZYGOSITY; HUMAN; INDIGENOUS PEOPLE; LRP5 GENE; POPULATION GENETIC STRUCTURE; PRKG1 GENE; RUSSIAN FEDERATION; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SMOOTH MUSCLE CONTRACTION; THADA GENE; VASCULAR SMOOTH MUSCLE; ACCLIMATIZATION; COLD CLIMATE; ETHNOLOGY; GENETICS; GENOMICS; MOLECULAR EVOLUTION; POPULATION GROUP;

ACCLIMATIZATION; COLD CLIMATE; EVOLUTION, MOLECULAR; GENOMICS; HUMANS; POLYMORPHISM, SINGLE NUCLEOTIDE; POPULATION GROUPS; SELECTION, GENETIC; SIBERIA;

EID: 84901372123     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0098076     Document Type: Article

References (68)

1. Goebel T (1999) Pleistocene human colonization of Siberia and peopling of the Americas: An ecological approach. Evolutionary Anthropology: Issues, News, and Reviews 8: 208-227.
2. Goebel T, Waters MR, O'Rourke DH (2008) The Late Pleistocene Dispersal of Modern Humans in the Americas. Science 319: 1497-1502. (Pubitemid 351398171)
3. Pitulko VV, Nikolsky PA, Girya EY, Basilyan AE, Tumskoy VE, et al. (2004) The Yana RHS site: humans in the Arctic before the last glacial maximum. Science 303: 52-56. (Pubitemid 38055765)
4. Richards MP, Pettitt PB, Stiner MC, Trinkaus E (2001) Stable isotope evidence for increasing dietary breadth in the European mid-Upper Paleolithic. Proceedings of the National Academy of Sciences 98: 6528-6532. (Pubitemid 32488271)
5. Clark PU, Dyke AS, Shakun JD, Carlson AE, Clark J, et al. (2009) The Last Glacial Maximum. Science 325: 710-714.
6. Kuzmin Y (2008) Siberia at the Last Glacial Maximum: Environment and Archaeology. Journal of Archaeological Research 16: 163-221.
7. Leonard WR, Snodgrass JJ, Sorensen MV (2005) Metabolic adaptations in indigenous Siberian populations. Annual Review of Anthropology 34: 451-471. (Pubitemid 41638316)
8. Bjerregaard P, Dewailly E, Young TK, Blanchet C, Hegele RA, et al. (2003) Blood pressure among the Inuit (Eskimo) populations in the Arctic. Scand J Public Health 31: 92-99. (Pubitemid 41007521)
9. Shephard RJ RA (1996) The Health Consequences of 'Modernisation': Evidence from Circumpolar Peoples. Cambridge: Cambridge University Press.
10. Snodgrass JJ, Leonard WR, Sorensen MV, Tarskaia LA, Mosher MJ (2008) The influence of basal metabolic rate on blood pressure among indigenous Siberians. Am J Phys Anthropol 137: 145-155.
11. The International HapMap Consortium (2005) A haplotype map of the human genome. Nature 437: 1299-1320.
12. 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)
13. Cann HM, de Toma C, Cazes L, Legrand MF, Morel V, et al. (2002) A human genome diversity cell line panel. Science 296: 261-262. (Pubitemid 34303653)
14. Genomes Project Consortium (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56-65.
15. Rasmussen M, Li Y, Lindgreen S, Pedersen JS, Albrechtsen A, et al. (2010) Ancient human genome sequence of an extinct Palaeo-Eskimo. Nature 463: 757-762.
16. Reich D, Patterson N, Campbell D, Tandon A, Mazieres S, et al. (2012) Reconstructing Native American population history. Nature 488: 370-374.
17. Hancock AM, Witonsky DB, Alkorta-Aranburu G, Beall CM, Gebremedhin A, et al. (2011) Adaptations to climate-mediated selective pressures in humans. PLoS Genet 7: e1001375.
18. Hancock AM, Witonsky DB, Gordon AS, Eshel G, Pritchard JK, et al. (2008) Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genet 4: e32.
19. Cannon B, Nedergaard J (2011) Nonshivering thermogenesis and its adequate measurement in metabolic studies. J Exp Biol 214: 242-253.
20. Frisancho AR (1993) Human adaptation and accommodation. Ann Arbor: University of Michigan Press.
21. De Lorenzo F, Sharma V, Scully M, Kakkar VV (1999) Cold adaptation and the seasonal distribution of acute myocardial infarction. QJM 92: 747-751.
22. LeBlanc J, Dulac S, Cote J, Girard B (1975) Autonomic nervous system and adaptation to cold in man. J Appl Physiol 39: 181-186.
23. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84: 277-359. (Pubitemid 38054374)
24. 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)
25. Delaneau O, Marchini J, Zagury JF (2012) A linear complexity phasing method for thousands of genomes. Nat Methods 9: 179-181.
26. 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.
27. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19: 1655-1664.
28. Lawson DJ, Falush D (2012) Population identification using genetic data. Annu Rev Genomics Hum Genet 13: 337-361.
29. Lawson DJ, Hellenthal G, Myers S, Falush D (2012) Inference of population structure using dense haplotype data. PLoS Genet 8: e1002453.
30. Pickrell JK, Pritchard JK (2012) Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet 8: e1002967.
31. Reich D, Thangaraj K, Patterson N, Price AL, Singh L (2009) Reconstructing Indian population history. Nature 461: 489-494.
32. Loh PR, Lipson M, Patterson N, Moorjani P, Pickrell JK, et al. (2013) Inferring admixture histories of human populations using linkage disequilibrium. Genetics 193: 1233-1254.
33. Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4: e72.
34. 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.
35. 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.
36. Weir BS, Cockerham CC (1984) Estimating F-Statistics for the Analysis of Population Structure. Evolution 38: 1358-1370. (Pubitemid 16277759)
37. Cockerham CC (1973) Analyses of gene frequencies. Genetics 74: 679-700.
38. Rousset F (2008) genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8: 103-106.
39. Wickham H (2009) ggplot2: elegant graphics for data analysis: Springer New York.
40. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
41. R Core Team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
42. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29. (Pubitemid 30257031)
43. Huang dW, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13.
44. Huang dW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
45. Lee JM, Sonnhammer EL (2003) Genomic gene clustering analysis of pathways in eukaryotes. Genome Res 13: 875-882. (Pubitemid 36621748)
46. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate - A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57: 289-300.
47. Blüthgen N, Brand K, Cajavec B, Swat M, Herzel H, et al. (2005) Biological profiling of gene groups utilizing Gene Ontology. Genome Inform 16: 106-115.
48. Winkler CA, Nelson GW, Smith MW (2010) Admixture mapping comes of age. Annu Rev Genomics Hum Genet 11: 65-89.
49. Metspalu M, Romero IG, Yunusbayev B, Chaubey G, Mallick CB, et al. (2011) Shared and unique components of human population structure and genomewide signals of positive selection in South Asia. Am J Hum Genet 89: 731-744.
50. Chea J, Zhang S, Zhao H, Zhang Z, Lee EYC, et al. (2012) Spatiotemporal recruitment of human DNA polymerase delta to sites of UV damage. Cell Cycle 11: 2885-2895.
51. Fedorova SA, Reidla M, Metspalu E, Metspalu M, Rootsi S, et al. (2013) Autosomal and uniparental portraits of the native populations of Sakha (Yakutia): implications for the peopling of Northeast Eurasia. BMC Evol Biol 13: 127.
52. Pritchard JK, Pickrell JK, Coop G (2010) The genetics of human adaptation: hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol 20: R208-215.
53. Turchin MC, Chiang CW, Palmer CD, Sankararaman S, Reich D, et al. (2012) Evidence of widespread selection on standing variation in Europe at height-associated SNPs. Nat Genet 44: 1015-1019.
54. Gong Y, Slee RB, Fukai N, Rawadi G, Roman-Roman S, et al. (2001) LDL receptor-related protein 5 (LRP5) affects bone accrual and eye development. Cell 107: 513-523. (Pubitemid 33152786)
55. Lappalainen S, Saarinen A, Utriainen P, Voutilainen R, Jääskeläinen J, et al. (2009) LRP5 in premature adrenarche and in metabolic characteristics of prepubertal children. Clin Endocrinol (Oxf) 70: 725-731.
56. Phinney SD (2004) Ketogenic diets and physical performance. Nutr Metab (Lond) 1: 2.
57. Reynolds JE, Wetzel DL, Hara TM (2009) Human Health Implications of Omega-3 and Omega-6 Fatty Acids in Blubber of the Bowhead Whale (Balaena mysticetus). Arctic 59.
58. M. G. Levin LPP (1964) The Peoples of Siberia. United States of America: University of Chicago.
59. Enattah NS, Sahi T, Savilahti E, Terwilliger JD, Peltonen L, et al. (2002) Identification of a variant associated with adult-type hypolactasia. Nat Genet 30: 233-237.
60. Kennedy AR, Pissios P, Otu H, Roberson R, Xue B, et al. (2007) A high-fat, ketogenic diet induces a unique metabolic state in mice. Am J Physiol Endocrinol Metab 292: E1724-1739. (Pubitemid 47084708)
61. Cannon B, Nedergaard J (2010) Thyroid hormones: igniting brown fat via the brain. Nat Med 16: 965-967.
62. Schreurs M, Kuipers F, van der Leij FR (2010) Regulatory enzymes of mitochondrial beta-oxidation as targets for treatment of the metabolic syndrome. Obes Rev 11: 380-388.
63. Franceschini N, Haack K, Göring HH, Voruganti VS, Laston S, et al. (2013) Epidemiology and genetic determinants of progressive deterioration of glycaemia in American Indians: the Strong Heart Family Study. Diabetologia.
64. Zeggini E, Scott LJ, Saxena R, Voight BF, Marchini JL, et al. (2008) Metaanalysis of genome-wide association data and large-scale replication identifies additional susceptibility loci for type 2 diabetes. Nat Genet 40: 638-645. (Pubitemid 351601209)
65. Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, et al. (2010) A draft sequence of the Neandertal genome. Science 328: 710-722.
66. Lincoln TM, Dey N, Sellak H (2001) Invited review: cGMP-dependent protein kinase signaling mechanisms in smooth muscle: from the regulation of tone to gene expression. J Appl Physiol 91: 1421-1430. (Pubitemid 32803941)
67. Kim HR, Appel S, Vetterkind S, Gangopadhyay SS, Morgan KG (2008) Smooth muscle signalling pathways in health and disease. J Cell Mol Med 12: 2165-2180.
68. Beall CM (2006) Andean, Tibetan, and Ethiopian patterns of adaptation to highaltitude hypoxia. Integr Comp Biol 46: 18-24.