Global Landscapes of Human Phenotypic Variation in Inherited Traits

Chapter
Part of the Evolutionary Studies book series (EVOLUS)

Abstract

Modern humans exhibit phenotypic variation among individuals, and phenotypes in some physical and physiological traits are highly differentiated between populations. This chapter focuses on genetic polymorphisms related to phenotypes that show interpopulation differentiation, which have traditionally attracted the attention of both anthropologists and human geneticists. Owing to the recent development of DNA technology, we have obtained powerful tools for use in identifying the genetic polymorphisms associated with phenotypes. In addition, the availability of genome diversity data associated with global populations has enabled us to identify the signatures of the local genetic adaptations that are engraved in our genomes. Using data associated with current phenotypic variation in humans, we can elucidate the history of human adaptation in response to the selective pressures of various environments.

Keywords

Phenotypic variation Genetic differentiation Genetic adaptation Selective sweep Genome-wide association study Physical and physiological traits 

References

  1. Adhikari K et al (2015) A genome-wide association study identifies multiple loci for variation in human ear morphology. Nat Commun 6:7500PubMedPubMedCentralCrossRefGoogle Scholar
  2. Akey JM, Wang H, Xiong M, Wu H, Liu W, Shriver MD, Jin L (2001) Interaction between the melanocortin-1 receptor and P genes contributes to inter-individual variation in skin pigmentation phenotypes in a Tibetan population. Hum Genet 108(6):516–520PubMedCrossRefGoogle Scholar
  3. Amundadottir L et al (2009) Genome-wide association study identifies variants in the ABO locus associated with susceptibility to pancreatic cancer. Nat Genet 41(9):986–990PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aoki K (2002) Sexual selection as a cause of human skin colour variation: Darwin’s hypothesis revisited. Ann Hum Biol 29(6):589–608PubMedCrossRefGoogle Scholar
  5. Arifuzzaman M et al (2011) Individuals with Le(a+b−) blood group have increased susceptibility to symptomatic vibrio cholerae O1 infection. PLoS Negl Trop Dis 5(12):e1413PubMedPubMedCentralCrossRefGoogle Scholar
  6. Band G et al (2013) Imputation-based meta-analysis of severe malaria in three African populations. PLoS Genet 9(5):e1003509PubMedPubMedCentralCrossRefGoogle Scholar
  7. Barbalic M et al (2010) Large-scale genomic studies reveal central role of ABO in sP-selectin and sICAM-1 levels. Hum Mol Genet 19(9):1863–1872PubMedPubMedCentralCrossRefGoogle Scholar
  8. Beja-Pereira A et al (2003) Gene-culture coevolution between cattle milk protein genes and human lactase genes. Nat Genet 35(4):311–313PubMedCrossRefGoogle Scholar
  9. Berndt SI et al (2013) Genome-wide meta-analysis identifies 11 new loci for anthropometric traits and provides insights into genetic architecture. Nat Genet 45(5):501–512PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bersaglieri T, Sabeti PC, Patterson N, Vanderploeg T, Schaffner SF, Drake JA, Rhodes M, Reich DE, Hirschhorn JN (2004) Genetic signatures of strong recent positive selection at the lactase gene. Am J Hum Genet 74(6):1111–1120PubMedPubMedCentralCrossRefGoogle Scholar
  11. Blackwell CC, Jonsdottir K, Hanson MF, Weir DM (1986a) Non-secretion of ABO blood group antigens predisposing to infection by Haemophilus influenzae. Lancet 2(8508):687PubMedCrossRefGoogle Scholar
  12. Blackwell CC, Jonsdottir K, Hanson M, Todd WT, Chaudhuri AK, Mathew B, Brettle RP, Weir DM (1986b) Non-secretion of ABO antigens predisposing to infection by Neisseria meningitidis and Streptococcus pneumoniae. Lancet 2(8501):284–285PubMedCrossRefGoogle Scholar
  13. Blackwell CC, Dundas S, James VS, Mackenzie DA, Braun JM, Alkout AM, Todd WT, Elton RA, Weir DM (2002) Blood group and susceptibility to disease caused by Escherichia coli O157. J Infect Dis 185(3):393–396PubMedCrossRefGoogle Scholar
  14. Boyko AR (2011) The domestic dog: man’s best friend in the genomic era. Genome Biol 12(2):216PubMedPubMedCentralCrossRefGoogle Scholar
  15. Brockschmidt FF et al (2011) Susceptibility variants on chromosome 7p21.1 suggest HDAC9 as a new candidate gene for male-pattern baldness. Br J Dermatol 165(6):1293–1302PubMedCrossRefGoogle Scholar
  16. Calafell F, Roubinet F, Ramirez-Soriano A, Saitou N, Bertranpetit J, Blancher A (2008) Evolutionary dynamics of the human ABO gene. Hum Genet 124(2):123–135PubMedCrossRefGoogle Scholar
  17. Chambers JC et al (2011) Genome-wide association study identifies loci influencing concentrations of liver enzymes in plasma. Nat Genet 43(11):1131–1138PubMedPubMedCentralCrossRefGoogle Scholar
  18. Chery C et al (2013) Gastric intrinsic factor deficiency with combined GIF heterozygous mutations and FUT2 secretor variant. Biochimie 95(5):995–1001PubMedCrossRefGoogle Scholar
  19. Claes P et al (2014) Modeling 3D facial shape from DNA. PLoS Genet 10(3):e1004224PubMedPubMedCentralCrossRefGoogle Scholar
  20. Clemens JD et al (1989) ABO blood groups and cholera: new observations on specificity of risk and modification of vaccine efficacy. J Infect Dis 159(4):770–773PubMedCrossRefGoogle Scholar
  21. Clemente FJ et al (2014) A selective sweep on a deleterious mutation in CPT1A in Arctic populations. Am J Hum Genet 95(5):584–589PubMedPubMedCentralCrossRefGoogle Scholar
  22. Currat M, Trabuchet G, Rees D, Perrin P, Harding RM, Clegg JB, Langaney A, Excoffier L (2002) Molecular analysis of the beta-globin gene cluster in the Niokholo Mandenka population reveals a recent origin of the beta(S) Senegal mutation. Am J Hum Genet 70(1):207–223PubMedCrossRefGoogle Scholar
  23. Daub JT, Hofer T, Cutivet E, Dupanloup I, Quintana-Murci L, Robinson-Rechavi M, Excoffier L (2013) Evidence for polygenic adaptation to pathogens in the human genome. Mol Biol Evol 30(7):1544–1558PubMedCrossRefGoogle Scholar
  24. Dichgans M et al (2014) Shared genetic susceptibility to ischemic stroke and coronary artery disease: a genome-wide analysis of common variants. Stroke 45(1):24–36PubMedCrossRefGoogle Scholar
  25. Eastlund T (1998) The histo-blood group ABO system and tissue transplantation. Transfusion 38(10):975–988PubMedCrossRefGoogle Scholar
  26. Edenberg HJ (2000) Regulation of the mammalian alcohol dehydrogenase genes. Prog Nucleic Acid Res Mol Biol 64:295–341PubMedCrossRefGoogle Scholar
  27. Edgren G, Hjalgrim H, Rostgaard K, Norda R, Wikman A, Melbye M, Nyren O (2010) Risk of gastric cancer and peptic ulcers in relation to ABO blood type: a cohort study. Am J Epidemiol 172(11):1280–1285PubMedCrossRefGoogle Scholar
  28. Edwards M, Bigham A, Tan J, Li S, Gozdzik A, Ross K, Jin L, Parra EJ (2010) Association of the OCA2 polymorphism His615Arg with melanin content in east Asian populations: further evidence of convergent evolution of skin pigmentation. PLoS Genet 6(3):e1000867PubMedPubMedCentralCrossRefGoogle Scholar
  29. Ellis JA, Stebbing M, Harrap SB (2001) Polymorphism of the androgen receptor gene is associated with male pattern baldness. J Invest Dermatol 116(3):452–455PubMedCrossRefGoogle Scholar
  30. Enattah NS, Sahi T, Savilahti E, Terwilliger JD, Peltonen L, Jarvela I (2002) Identification of a variant associated with adult-type hypolactasia. Nat Genet 30(2):233–237PubMedCrossRefGoogle Scholar
  31. Eriksson N et al (2010) Web-based, participant-driven studies yield novel genetic associations for common traits. PLoS Genet 6(6):e1000993PubMedPubMedCentralCrossRefGoogle Scholar
  32. Ferrer-Admetlla A, Sikora M, Laayouni H, Esteve A, Roubinet F, Blancher A, Calafell F, Bertranpetit J, Casals F (2009) A natural history of FUT2 polymorphism in humans. Mol Biol Evol 26(9):1993–2003PubMedCrossRefGoogle Scholar
  33. Franbourg A, Hallegot P, Baltenneck F, Toutain C, Leroy F (2003) Current research on ethnic hair. J Am Acad Dermatol 48(6 Suppl):S115–S119PubMedCrossRefGoogle Scholar
  34. Frank J et al (2012) Genome-wide significant association between alcohol dependence and a variant in the ADH gene cluster. Addict Biol 17(1):171–180PubMedCrossRefGoogle Scholar
  35. Franke A et al (2010) Genome-wide meta-analysis increases to 71 the number of confirmed Crohn’s disease susceptibility loci. Nat Genet 42(12):1118–1125PubMedPubMedCentralCrossRefGoogle Scholar
  36. Fujimoto A et al (2008) A scan for genetic determinants of human hair morphology: EDAR is associated with Asian hair thickness. Hum Mol Genet 17(6):835–843PubMedCrossRefGoogle Scholar
  37. Fumagalli M et al. (2011) Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLOS Genet 7:e1002355Google Scholar
  38. Fumagalli M et al (2015) Greenlandic Inuit show genetic signatures of diet and climate adaptation. Science 349(6254):1343–1347PubMedCrossRefGoogle Scholar
  39. Glass RI et al (1985) Predisposition for cholera of individuals with O blood group. Possible evolutionary significance. Am J Epidemiol 121(6):791–796PubMedCrossRefGoogle Scholar
  40. Goedde HW, Agarwal DP, Harada S, Meier-Tackmann D, Ruofu D, Bienzle U, Kroeger A, Hussein L (1983) Population genetic studies on aldehyde dehydrogenase isozyme deficiency and alcohol sensitivity. Am J Hum Genet 35(4):769–772PubMedPubMedCentralGoogle Scholar
  41. Goldman D, Enoch MA (1990) Genetic epidemiology of ethanol metabolic enzymes: a role for selection. World Rev Nutr Diet 63:143–160PubMedCrossRefGoogle Scholar
  42. Grossman SR et al (2010) A composite of multiple signals distinguishes causal variants in regions of positive selection. Science 327(5967):883–886PubMedCrossRefGoogle Scholar
  43. Grossman SR et al (2013) Identifying recent adaptations in large-scale genomic data. Cell 152(4):703–713PubMedPubMedCentralCrossRefGoogle Scholar
  44. Guo J et al (2014) Variation and signatures of selection on the human face. J Hum Evol 75:143–152Google Scholar
  45. Hamblin MT, Di Rienzo A (2000) Detection of the signature of natural selection in humans: evidence from the Duffy blood group locus. Am J Hum Genet 66(5):1669–1679PubMedPubMedCentralCrossRefGoogle Scholar
  46. Hamilton JB (1951) Patterned loss of hair in man; types and incidence. Ann N Y Acad Sci 53(3):708–728PubMedCrossRefGoogle Scholar
  47. Han J et al (2008) A genome-wide association study identifies novel alleles associated with hair color and skin pigmentation. PLoS Genet 4(5):e1000074PubMedPubMedCentralCrossRefGoogle Scholar
  48. Hancock AM, Witonsky DB, Gordon AS, Eshel G, Pritchard JK, Coop G, Di Rienzo A (2008) Adaptations to climate in candidate genes for common metabolic disorders. PLoS Genet 4(2):e32PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hancock AM et al (2011) Adaptations to climate-mediated selective pressures in humans. PLoS Genet 7(4):e1001375PubMedPubMedCentralCrossRefGoogle Scholar
  50. Harada S, Misawa S, Agarwal DP, Goedde HW (1980) Liver alcohol dehydrogenase and aldehyde dehydrogenase in the Japanese: isozyme variation and its possible role in alcohol intoxication. Am J Hum Genet 32(1):8–15PubMedPubMedCentralGoogle Scholar
  51. Harris JB et al (2005) Blood group, immunity, and risk of infection with Vibrio cholerae in an area of endemicity. Infect Immun 73(11):7422–7427PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hazra A, Kraft P, Selhub J, Giovannucci EL, Thomas G, Hoover RN, Chanock SJ, Hunter DJ (2008) Common variants of FUT2 are associated with plasma vitamin B12 levels. Nat Genet 40(10):1160–1162PubMedPubMedCentralCrossRefGoogle Scholar
  53. Hazra A, Kraft P, Lazarus R, Chen C, Chanock SJ, Jacques P, Selhub J, Hunter DJ (2009) Genome-wide significant predictors of metabolites in the one-carbon metabolism pathway. Hum Mol Genet 18(23):4677–4687PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hedrick PW, Whittam TS, Parham P (1991) Heterozygosity at individual amino acid sites: extremely high levels for HLA-A and -B genes. Proc Natl Acad Sci U S A 88(13):5897–5901PubMedPubMedCentralCrossRefGoogle Scholar
  55. Heit JA, Armasu SM, Asmann YW, Cunningham JM, Matsumoto ME, Petterson TM, De Andrade M (2012) A genome-wide association study of venous thromboembolism identifies risk variants in chromosomes 1q24.2 and 9q. J Thromb Haemost 10(8):1521–1531PubMedPubMedCentralCrossRefGoogle Scholar
  56. Hillmer AM et al (2008) Susceptibility variants for male-pattern baldness on chromosome 20p11. Nat Genet 40(11):1279–1281PubMedCrossRefGoogle Scholar
  57. Hillmer AM et al (2009) Recent positive selection of a human androgen receptor/ectodysplasin A2 receptor haplotype and its relationship to male pattern baldness. Hum Genet 126(2):255–264PubMedPubMedCentralCrossRefGoogle Scholar
  58. Huang L, Li Y, Singleton AB, Hardy JA, Abecasis G, Rosenberg NA, Scheet P (2009) Genotype-imputation accuracy across worldwide human populations. Am J Hum Genet 84(2):235–250PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hubbe M, Hanihara T, Harvati K (2009) Climate signatures in the morphological differentiation of worldwide modern human populations. Anat Rec-Adv Integr Anat Evol Biol 292(11):1720–1733CrossRefGoogle Scholar
  60. Hughes AL, Nei M (1988) Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335(6186):167–170PubMedCrossRefGoogle Scholar
  61. Hurley TD, Bosron WF, Stone CL, Amzel LM (1994) Structures of three human beta alcohol dehydrogenase variants. Correlations with their functional differences. J Mol Biol 239(3):415–429PubMedCrossRefGoogle Scholar
  62. Iodice S, Maisonneuve P, Botteri E, Sandri MT, Lowenfels AB (2010) ABO blood group and cancer. Eur J Cancer 46(18):3345–3350PubMedCrossRefGoogle Scholar
  63. Itan Y, Powell A, Beaumont MA, Burger J, Thomas MG (2009) The origins of lactase persistence in Europe. PLoS Comput Biol 5(8):e1000491PubMedPubMedCentralCrossRefGoogle Scholar
  64. Jablonski NG, Chaplin G (2000) The evolution of human skin coloration. J Hum Evol 39(1):57–106PubMedCrossRefGoogle Scholar
  65. Jarvis JP et al (2012) Patterns of ancestry, signatures of natural selection, and genetic association with stature in Western African pygmies. PLoS Genet 8(4):e1002641PubMedPubMedCentralCrossRefGoogle Scholar
  66. Jostins L et al (2012) Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491(7422):119–124PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kamatani Y, Matsuda K, Okada Y, Kubo M, Hosono N, Daigo Y, Nakamura Y, Kamatani N (2010) Genome-wide association study of hematological and biochemical traits in a Japanese population. Nat Genet 42(3):210–215PubMedCrossRefGoogle Scholar
  68. Kamberov YG et al (2013) Modeling recent human evolution in mice by expression of a selected EDAR variant. Cell 152(4):691–702PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kapoor M et al (2013) A meta-analysis of two genome-wide association studies to identify novel loci for maximum number of alcoholic drinks. Hum Genet 132(10):1141–1151PubMedPubMedCentralCrossRefGoogle Scholar
  70. Kelly RJ, Rouquier S, Giorgi D, Lennon GG, Lowe JB (1995) Sequence and expression of a candidate for the human secretor blood group alpha(1,2)fucosyltransferase gene (FUT2). Homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype. J Biol Chem 270(9):4640–4649PubMedCrossRefGoogle Scholar
  71. Kenny EE et al (2012) Melanesian blond hair is caused by an amino acid change in TYRP1. Science 336(6081):554PubMedPubMedCentralCrossRefGoogle Scholar
  72. Kim YJ et al (2011) Large-scale genome-wide association studies in East Asians identify new genetic loci influencing metabolic traits. Nat Genet 43(10):990–995PubMedCrossRefGoogle Scholar
  73. Kimura R, Fujimoto A, Tokunaga K, Ohashi J (2007) A practical genome scan for population-specific strong selective sweeps that have reached fixation. PLoS One 2(3):e286PubMedPubMedCentralCrossRefGoogle Scholar
  74. Kimura R, Ohashi J, Matsumura Y, Nakazawa M, Inaoka T, Ohtsuka R, Osawa M, Tokunaga K (2008) Gene flow and natural selection in oceanic human populations inferred from genome-wide SNP typing. Mol Biol Evol 25(8):1750–1761PubMedCrossRefGoogle Scholar
  75. Kimura R et al (2009) A common variation in EDAR is a genetic determinant of shovel-shaped incisors. Am J Hum Genet 85(4):528–535PubMedPubMedCentralCrossRefGoogle Scholar
  76. Koda Y, Soejima M, Liu Y, Kimura H (1996) Molecular basis for secretor type alpha(1,2)-fucosyltransferase gene deficiency in a Japanese population: a fusion gene generated by unequal crossover responsible for the enzyme deficiency. Am J Hum Genet 59(2):343–350PubMedPubMedCentralGoogle Scholar
  77. Koda Y, Soejima M, Johnson PH, Smart E, Kimura H (2000a) An Alu-mediated large deletion of the FUT2 gene in individuals with the ABO-Bombay phenotype. Hum Genet 106(1):80–85PubMedCrossRefGoogle Scholar
  78. Koda Y, Tachida H, Soejima M, Takenaka O, Kimura H (2000b) Ancient origin of the null allele se(428) of the human ABO-secretor locus (FUT2). J Mol Evol 50(3):243–248PubMedCrossRefGoogle Scholar
  79. Koda Y, Tachida H, Pang H, Liu Y, Soejima M, Ghaderi AA, Takenaka O, Kimura H (2001) Contrasting patterns of polymorphisms at the ABO-secretor gene (FUT2) and plasma alpha(1,3)fucosyltransferase gene (FUT6) in human populations. Genetics 158(2):747–756PubMedPubMedCentralGoogle Scholar
  80. Kudo T, Iwasaki H, Nishihara S, Shinya N, Ando T, Narimatsu I, Narimatsu H (1996) Molecular genetic analysis of the human Lewis histo-blood group system. II. Secretor gene inactivation by a novel single missense mutation A385T in Japanese nonsecretor individuals. J Biol Chem 271(16):9830–9837PubMedCrossRefGoogle Scholar
  81. Lango Allen H et al (2010) Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature 467(7317):832–838PubMedPubMedCentralCrossRefGoogle Scholar
  82. Lao O, de Gruijter JM, van Duijn K, Navarro A, Kayser M (2007) Signatures of positive selection in genes associated with human skin pigmentation as revealed from analyses of single nucleotide polymorphisms. Ann Hum Genet 71(Pt 3):354–369PubMedCrossRefGoogle Scholar
  83. Leinonen T, McCairns RJ, O'Hara RB, Merila J (2013) Q(ST)-F(ST) comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat Rev Genet 14(3):179–190PubMedCrossRefGoogle Scholar
  84. Li H et al (2007) Geographically separate increases in the frequency of the derived ADH1B*47His allele in eastern and western Asia. Am J Hum Genet 81(4):842–846PubMedPubMedCentralCrossRefGoogle Scholar
  85. Li R et al (2012) Six novel susceptibility loci for early-onset androgenetic alopecia and their unexpected association with common diseases. PLoS Genet 8(5):e1002746PubMedPubMedCentralCrossRefGoogle Scholar
  86. Li J et al (2013) Genome-wide association study on serum alkaline phosphatase levels in a Chinese population. BMC Genomics 14:684PubMedPubMedCentralCrossRefGoogle Scholar
  87. Lin X et al (2012) Genome-wide association study identifies novel loci associated with serum level of vitamin B12 in Chinese men. Hum Mol Genet 21(11):2610–2617PubMedCrossRefGoogle Scholar
  88. Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, Lindblad L, Stewart P, LePendu J, Baric R (2003) Human susceptibility and resistance to Norwalk virus infection. Nat Med 9(5):548–553PubMedCrossRefGoogle Scholar
  89. Liu F et al (2012) A genome-wide association study identifies five loci influencing facial morphology in Europeans. PLoS Genet 8(9):e1002932PubMedPubMedCentralCrossRefGoogle Scholar
  90. Liumbruno GM, Franchini M (2013) Beyond immunohaematology: the role of the ABO blood group in human diseases. Blood Transfus = Trasfusione del sangue 11(4):491–499PubMedGoogle Scholar
  91. Macgregor S et al (2009) Associations of ADH and ALDH2 gene variation with self report alcohol reactions, consumption and dependence: an integrated analysis. Hum Mol Genet 18(3):580–593PubMedCrossRefGoogle Scholar
  92. Maes HH, Neale MC, Eaves LJ (1997) Genetic and environmental factors in relative body weight and human adiposity. Behav Genet 27(4):325–351PubMedCrossRefGoogle Scholar
  93. Matsunaga E (1962) The dimorphism in human normal cerumen. Ann Hum Genet 25:273–286PubMedCrossRefGoogle Scholar
  94. McCarthy MI, Abecasis GR, Cardon LR, Goldstein DB, Little J, Ioannidis JP, Hirschhorn JN (2008) Genome-wide association studies for complex traits: consensus, uncertainty and challenges. Nat Rev Genet 9(5):356–369PubMedCrossRefGoogle Scholar
  95. McGovern DP et al (2010) Fucosyltransferase 2 (FUT2) non-secretor status is associated with Crohn’s disease. Hum Mol Genet 19(17):3468–3476PubMedPubMedCentralCrossRefGoogle Scholar
  96. Medland SE et al (2009) Common variants in the trichohyalin gene are associated with straight hair in Europeans. Am J Hum Genet 85(5):750–755PubMedPubMedCentralCrossRefGoogle Scholar
  97. Miura K et al (2007) A strong association between human earwax-type and apocrine colostrum secretion from the mammary gland. Hum Genet 121(5):631–633PubMedCrossRefGoogle Scholar
  98. Moeller A, Weippert-Kretschmer M, Prinz H, Kretschmer V (2001) Influence of ABO blood groups on primary hemostasis. Transfusion 41(1):56–60PubMedCrossRefGoogle Scholar
  99. Moltke I et al (2014) A common Greenlandic TBC1D4 variant confers muscle insulin resistance and type 2 diabetes. Nature 512(7513):190–193PubMedCrossRefGoogle Scholar
  100. Nakano M, Miwa N, Hirano A, Yoshiura K, Niikawa N (2009) A strong association of axillary osmidrosis with the wet earwax type determined by genotyping of the ABCC11 gene. BMC Genet 10:42PubMedPubMedCentralCrossRefGoogle Scholar
  101. Nan H, Kraft P, Hunter DJ, Han J (2009) Genetic variants in pigmentation genes, pigmentary phenotypes, and risk of skin cancer in Caucasians. Int J Cancer 125(4):909–917PubMedPubMedCentralCrossRefGoogle Scholar
  102. Neel JV (1962) Diabetes mellitus: a “thrifty” genotype rendered detrimental by “progress”? Am J Hum Genet 14:353–362PubMedPubMedCentralGoogle Scholar
  103. Norton HL et al (2007) Genetic evidence for the convergent evolution of light skin in Europeans and East Asians. Mol Biol Evol 24(3):710–722PubMedCrossRefGoogle Scholar
  104. O’Donnell J, Laffan MA (2001) The relationship between ABO histo-blood group, factor VIII and von Willebrand factor. Transfus Med 11(4):343–351PubMedCrossRefGoogle Scholar
  105. Ohashi J, Naka I, Patarapotikul J, Hananantachai H, Brittenham G, Looareesuwan S, Clark AG, Tokunaga K (2004) Extended linkage disequilibrium surrounding the hemoglobin E variant due to malarial selection. Am J Hum Genet 74(6):1198–1208PubMedPubMedCentralCrossRefGoogle Scholar
  106. Ohashi J, Naka I, Tsuchiya N (2011) The impact of natural selection on an ABCC11 SNP determining earwax type. Mol Biol Evol 28(1):849–857PubMedCrossRefGoogle Scholar
  107. Oota H et al (2004) The evolution and population genetics of the ALDH2 locus: random genetic drift, selection, and low levels of recombination. Ann Hum Genet 68(Pt 2):93–109PubMedCrossRefGoogle Scholar
  108. Oriol R, Le Pendu J, Sparkes RS, Sparkes MC, Crist M, Gale RP, Terasaki PI, Bernoco M (1981) Insights into the expression of ABH and Lewis antigens through human bone marrow transplantation. Am J Hum Genet 33(4):551–560PubMedPubMedCentralGoogle Scholar
  109. Osier MV et al (2002) A global perspective on genetic variation at the ADH genes reveals unusual patterns of linkage disequilibrium and diversity. Am J Hum Genet 71(1):84–99PubMedPubMedCentralCrossRefGoogle Scholar
  110. Pare G, Chasman DI, Kellogg M, Zee RY, Rifai N, Badola S, Miletich JP, Ridker PM (2008) Novel association of ABO histo-blood group antigen with soluble ICAM-1: results of a genome-wide association study of 6,578 women. PLoS Genet 4(7):e1000118PubMedPubMedCentralCrossRefGoogle Scholar
  111. Pare G et al (2011) Genome-wide association analysis of soluble ICAM-1 concentration reveals novel associations at the NFKBIK, PNPLA3, RELA, and SH2B3 loci. PLoS Genet 7(4):e1001374PubMedPubMedCentralCrossRefGoogle Scholar
  112. Park J et al (2012) Effects of an Asian-specific nonsynonymous EDAR variant on multiple dental traits. J Hum Genet in pressGoogle Scholar
  113. Park BL et al (2013) Extended genetic effects of ADH cluster genes on the risk of alcohol dependence: from GWAS to replication. Hum Genet 132(6):657–668PubMedCrossRefGoogle Scholar
  114. Paternoster L et al (2012) Genome-wide association study of three-dimensional facial morphology identifies a variant in PAX3 associated with nasion position. Am J Hum Genet 90(3):478–485PubMedPubMedCentralCrossRefGoogle Scholar
  115. Paterson AD et al (2009) Genome-wide association identifies the ABO blood group as a major locus associated with serum levels of soluble E-selectin. Arterioscler Thromb Vasc Biol 29(11):1958–1967PubMedPubMedCentralCrossRefGoogle Scholar
  116. Peng Y, Shi H, Qi XB, Xiao CJ, Zhong H, Ma RL, Su B (2010) The ADH1B Arg47His polymorphism in east Asian populations and expansion of rice domestication in history. BMC Evol Biol 10:15PubMedPubMedCentralCrossRefGoogle Scholar
  117. Peng S, Tan J, Hu S, Zhou H, Guo J, Jin L, Tang K (2013) Detecting genetic association of common human facial morphological variation using high density 3D image registration. PLoS Comput Biol 9(12):e1003375PubMedPubMedCentralCrossRefGoogle Scholar
  118. Pickrell JK et al (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res 19(5):826–837PubMedPubMedCentralCrossRefGoogle Scholar
  119. Plomin R, Haworth CM, Davis OS (2009) Common disorders are quantitative traits. Nat Rev Genet 10(12):872–878PubMedCrossRefGoogle Scholar
  120. Preston AE, Barr A (1964) The plasma concentration of factor Viii in the normal population. II. The effects of age, sex and blood group. Br J Haematol 10:238–245PubMedCrossRefGoogle Scholar
  121. Prugnolle F, Manica A, Charpentier M, Guegan JF, Guernier V, Balloux F (2005) Pathogen-driven selection and worldwide HLA class I diversity. Curr Biol 15(11):1022–1027PubMedCrossRefGoogle Scholar
  122. Qi L et al (2010) Genetic variants in ABO blood group region, plasma soluble E-selectin levels and risk of type 2 diabetes. Hum Mol Genet 19(9):1856–1862PubMedPubMedCentralCrossRefGoogle Scholar
  123. Ranciaro A et al (2014) Genetic origins of lactase persistence and the spread of pastoralism in Africa. Am J Hum Genet 94(4):496–510PubMedPubMedCentralCrossRefGoogle Scholar
  124. Rees JL (2003) Genetics of hair and skin color. Annu Rev Genet 37:67–90PubMedCrossRefGoogle Scholar
  125. Reilly MP et al (2011) Identification of ADAMTS7 as a novel locus for coronary atherosclerosis and association of ABO with myocardial infarction in the presence of coronary atherosclerosis: two genome-wide association studies. Lancet 377(9763):383–392PubMedPubMedCentralCrossRefGoogle Scholar
  126. Richards JB et al (2008) Male-pattern baldness susceptibility locus at 20p11. Nat Genet 40(11):1282–1284PubMedPubMedCentralCrossRefGoogle Scholar
  127. Risch HA, Yu H, Lu L, Kidd MS (2010) ABO blood group, Helicobacter pylori seropositivity, and risk of pancreatic cancer: a case-control study. J Natl Cancer Inst 102(7):502–505PubMedPubMedCentralCrossRefGoogle Scholar
  128. Roberts DF (1953) Body weight, race and climate. Am J Phys Anthropol 11(4):533–558PubMedCrossRefGoogle Scholar
  129. Roseman CC (2004) Detecting interregionally diversifying natural selection on modern human cranial form by using matched molecular and morphometric data. Proc Natl Acad Sci U S A 101(35):12824–12829PubMedPubMedCentralCrossRefGoogle Scholar
  130. Roseman CC, Weaver TD (2004) Multivariate apportionment of global human craniometric diversity. Am J Phys Anthropol 125(3):257–263PubMedCrossRefGoogle Scholar
  131. Rosenberg NA, Huang L, Jewett EM, Szpiech ZA, Jankovic I, Boehnke M (2010) Genome-wide association studies in diverse populations. Nat Rev Genet 11(5):356–366PubMedPubMedCentralCrossRefGoogle Scholar
  132. Rouquier S, Lowe JB, Kelly RJ, Fertitta AL, Lennon GG, Giorgi D (1995) Molecular cloning of a human genomic region containing the H blood group alpha(1,2)fucosyltransferase gene and two H locus-related DNA restriction fragments. Isolation of a candidate for the human secretor blood group locus. J Biol Chem 270(9):4632–4639PubMedCrossRefGoogle Scholar
  133. Roychoudhury AK, Nei M (1988) Human polymorphic genes: world distribution. Oxford University Press, New YorkGoogle Scholar
  134. Sabeti PC et al (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419(6909):832–837PubMedCrossRefGoogle Scholar
  135. Sabeti PC et al (2007) Genome-wide detection and characterization of positive selection in human populations. Nature 449(7164):913–918PubMedPubMedCentralCrossRefGoogle Scholar
  136. Schunkert H et al (2011) Large-scale association analysis identifies 13 new susceptibility loci for coronary artery disease. Nat Genet 43(4):333–338PubMedPubMedCentralCrossRefGoogle Scholar
  137. Scott GR, Turner CGI (1997) The anthropology of modern human teeth: dental morphology and its variation in recent human populations. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  138. Shai I, Jiang R, Manson JE, Stampfer MJ, Willett WC, Colditz GA, Hu FB (2006) Ethnicity, obesity, and risk of type 2 diabetes in women: a 20-year follow-up study. Diabetes Care 29(7):1585–1590PubMedCrossRefGoogle Scholar
  139. Sheinfeld J, Schaeffer AJ, Cordon-Cardo C, Rogatko A, Fair WR (1989) Association of the Lewis blood-group phenotype with recurrent urinary tract infections in women. N Engl J Med 320(12):773–777PubMedCrossRefGoogle Scholar
  140. Shibuya A, Yoshida A (1988) Genotypes of alcohol-metabolizing enzymes in Japanese with alcohol liver diseases: a strong association of the usual Caucasian-type aldehyde dehydrogenase gene (ALDH1(2)) with the disease. Am J Hum Genet 43(5):744–748PubMedPubMedCentralGoogle Scholar
  141. Skoglund P, Gotherstrom A, Jakobsson M (2011) Estimation of population divergence times from non-overlapping genomic sequences: examples from dogs and wolves. Mol Biol Evol 28(4):1505–1517PubMedCrossRefGoogle Scholar
  142. Stokowski RP et al (2007) A genomewide association study of skin pigmentation in a South Asian population. Am J Hum Genet 81(6):1119–1132PubMedPubMedCentralCrossRefGoogle Scholar
  143. Stunkard AJ, Foch TT, Hrubec Z (1986) A twin study of human obesity. JAMA 256(1):51–54PubMedCrossRefGoogle Scholar
  144. Sturm RA, Duffy DL (2012) Human pigmentation genes under environmental selection. Genome Biol 13(9):248PubMedPubMedCentralCrossRefGoogle Scholar
  145. Sulem P et al (2007) Genetic determinants of hair, eye and skin pigmentation in Europeans. Nat Genet 39(12):1443–1452PubMedCrossRefGoogle Scholar
  146. Sulem P et al (2008) Two newly identified genetic determinants of pigmentation in Europeans. Nat Genet 40(7):835–837PubMedCrossRefGoogle Scholar
  147. Takahata N, Satta Y, Klein J (1992) Polymorphism and balancing selection at major histocompatibility complex loci. Genetics 130(4):925–938PubMedPubMedCentralGoogle Scholar
  148. Tanaka T et al (2009) Genome-wide association study of vitamin B6, vitamin B12, folate, and homocysteine blood concentrations. Am J Hum Genet 84(4):477–482PubMedPubMedCentralCrossRefGoogle Scholar
  149. Tang K, Thornton KR, Stoneking M (2007) A new approach for using genome scans to detect recent positive selection in the human genome. PLoS Biol 5(7):–e171Google Scholar
  150. Tang W et al (2012) Genetic associations for activated partial thromboplastin time and prothrombin time, their gene expression profiles, and risk of coronary artery disease. Am J Hum Genet 91(1):152–162PubMedPubMedCentralCrossRefGoogle Scholar
  151. Tang W et al (2013) A genome-wide association study for venous thromboembolism: the extended cohorts for heart and aging research in genomic epidemiology (CHARGE) consortium. Genet Epidemiol 37(5):512–521PubMedPubMedCentralCrossRefGoogle Scholar
  152. Teslovich TM et al (2010) Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466(7307):707–713PubMedPubMedCentralCrossRefGoogle Scholar
  153. Timmann C et al (2012) Genome-wide association study indicates two novel resistance loci for severe malaria. Nature 489(7416):443–446PubMedCrossRefGoogle Scholar
  154. Tishkoff SA et al (2007) Convergent adaptation of human lactase persistence in Africa and Europe. Nat Genet 39(1):31–40PubMedCrossRefGoogle Scholar
  155. Tregouet DA et al (2009) Common susceptibility alleles are unlikely to contribute as strongly as the FV and ABO loci to VTE risk: results from a GWAS approach. Blood 113(21):5298–5303PubMedCrossRefGoogle Scholar
  156. van Loon FP et al (1991) ABO blood groups and the risk of diarrhea due to enterotoxigenic Escherichia coli. J Infect Dis 163(6):1243–1246PubMedCrossRefGoogle Scholar
  157. Voight BF, Kudaravalli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4(3):e72PubMedPubMedCentralCrossRefGoogle Scholar
  158. Wang ET, Kodama G, Baldi P, Moyzis RK (2006) Global landscape of recent inferred Darwinian selection for homo sapiens. Proc Natl Acad Sci U S A 103(1):135–140Google Scholar
  159. Wang TL et al (2010) Prevalence of androgenetic alopecia in China: a community-based study in six cities. Br J Dermatol 162(4):843–847PubMedCrossRefGoogle Scholar
  160. Wang Z, Liu L, Ji J, Zhang J, Yan M, Liu B, Zhu Z, Yu Y (2012) ABO blood group system and gastric cancer: a case-control study and meta-analysis. Int J Mol Sci 13(10):13308–13321PubMedPubMedCentralCrossRefGoogle Scholar
  161. Wen CP, David Cheng TY, Tsai SP, Chan HT, Hsu HL, Hsu CC, Eriksen MP (2009) Are Asians at greater mortality risks for being overweight than Caucasians? Redefining obesity for Asians. Public Health Nutr 12(4):497–506PubMedCrossRefGoogle Scholar
  162. Whitlock MC (2008) Evolutionary inference from QST. Mol Ecol 17(8):1885–1896PubMedCrossRefGoogle Scholar
  163. Willer CJ et al (2009) Six new loci associated with body mass index highlight a neuronal influence on body weight regulation. Nat Genet 41(1):25–34PubMedCrossRefGoogle Scholar
  164. Willer CJ et al (2013) Discovery and refinement of loci associated with lipid levels. Nat Genet 45(11):1274–1283PubMedPubMedCentralCrossRefGoogle Scholar
  165. Williams FM et al (2013) Ischemic stroke is associated with the ABO locus: the EuroCLOT study. Ann Neurol 73(1):16–31PubMedPubMedCentralCrossRefGoogle Scholar
  166. Williamson SH, Hubisz MJ, Clark AG, Payseur BA, Bustamante CD, Nielsen R (2007) Localizing recent adaptive evolution in the human genome. PLoS Genet 3(6):e90PubMedPubMedCentralCrossRefGoogle Scholar
  167. Wolpin BM, Chan AT, Hartge P, Chanock SJ, Kraft P, Hunter DJ, Giovannucci EL, Fuchs CS (2009) ABO blood group and the risk of pancreatic cancer. J Natl Cancer Inst 101(6):424–431PubMedPubMedCentralCrossRefGoogle Scholar
  168. Wood AR et al (2014) Defining the role of common variation in the genomic and biological architecture of adult human height. Nat Genet 46(11):1173–1186PubMedPubMedCentralCrossRefGoogle Scholar
  169. Yamaguchi K et al (2012) Association of melanocortin 1 receptor gene (MC1R) polymorphisms with skin reflectance and freckles in Japanese. J Hum Genet 57(11):700–708PubMedCrossRefGoogle Scholar
  170. Yamamoto F, Clausen H, White T, Marken J, Hakomori S (1990) Molecular genetic basis of the histo-blood group ABO system. Nature 345(6272):229–233PubMedCrossRefGoogle Scholar
  171. Yokoyama A, Tsutsumi E, Imazeki H, Suwa Y, Nakamura C, Yokoyama T (2007) Contribution of the alcohol dehydrogenase-1B genotype and oral microorganisms to high salivary acetaldehyde concentrations in Japanese alcoholic men. Int J Cancer 121(5):1047–1054PubMedCrossRefGoogle Scholar
  172. Yoshiura K et al (2006) A SNP in the ABCC11 gene is the determinant of human earwax type. Nat Genet 38(3):324–330PubMedCrossRefGoogle Scholar
  173. Young JM, Massa HF, Hsu L, Trask BJ (2010) Extreme variability among mammalian V1R gene families. Genome Res 20(1):10–18PubMedPubMedCentralCrossRefGoogle Scholar
  174. Yuan X et al (2008) Population-based genome-wide association studies reveal six loci influencing plasma levels of liver enzymes. Am J Hum Genet 83(4):520–528PubMedPubMedCentralCrossRefGoogle Scholar
  175. Zhou L et al (2013) A genome wide association study identifies common variants associated with lipid levels in the Chinese population. PLoS One 8(12):e82420PubMedPubMedCentralCrossRefGoogle Scholar
  176. Zimmerman PA et al (1999) Emergence of FY*A(null) in a plasmodium vivax-endemic region of Papua New Guinea. Proc Natl Acad Sci U S A 96(24):13973–13977PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Japan KK 2017

Authors and Affiliations

  1. 1.Department of Human Biology and Anatomy, Graduate School of MedicineUniversity of the RyukyusNishihara-choJapan

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