The Light Skin Allele of in South Asians and Europeans Shares Identity by Descent

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Skin pigmentation is one of the most variable phenotypic traits in humans. A non-synonymous substitution (rs1426654) in the third exon of SLC24A5 accounts for lighter skin in Europeans but not in East Asians. A previous genome-wide association study carried out in a heterogeneous sample of UK immigrants of South Asian descent suggested that this gene also contributes significantly to skin pigmentation variation among South Asians. In the present study, we have quantitatively assessed skin pigmentation for a largely homogeneous cohort of 1228 individuals from the Southern region of the Indian subcontinent. Our data confirm significant association of rs1426654 SNP with skin pigmentation, explaining about 27% of total phenotypic variation in the cohort studied. Our extensive survey of the polymorphism in 1573 individuals from 54 ethnic populations across the Indian subcontinent reveals wide presence of the derived-A allele, although the frequencies vary substantially among populations. We also show that the geospatial pattern of this allele is complex, but most importantly, reflects strong influence of language, geography and demographic history of the populations. Sequencing 11.74 kb of SLC24A5 in 95 individuals worldwide reveals that the rs1426654-A alleles in South Asian and West Eurasian populations are monophyletic and occur on the background of a common haplotype that is characterized by low genetic diversity. We date the coalescence of the light skin associated allele at 22–28 KYA. Both our sequence and genome-wide genotype data confirm that this gene has been a target for positive selection among Europeans. However, the latter also shows additional evidence of selection in populations of the Middle East, Central Asia, Pakistan and North India but not in South India.

Vyšlo v časopise: The Light Skin Allele of in South Asians and Europeans Shares Identity by Descent. PLoS Genet 9(11): e32767. doi:10.1371/journal.pgen.1003912
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003912

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Zdroje

1. ReesJL (2004) The genetics of sun sensitivity in humans. Am J Hum Genet 75 : 739–751.

2. ThodyAJ, HigginsEM, WakamatsuK, ItoS, BurchillSA, et al. (1991) Pheomelanin as well as eumelanin is present in human epidermis. J Invest Dermatol 97 : 340–344.

3. BarshGS (2003) What controls variation in human skin color. PLoS Biol 1: e27.

4. LamasonRL, MohideenMAPK, MestJR, WongAC, NortonHL, et al. (2005) SLC24A5, a putative cation exchanger, affects pigmentation in zebrafish and humans. Science 310 : 1782.

5. CandilleSI, AbsherDM, BelezaS, BauchetM, McEvoyB, et al. (2012) Genome-Wide Association Studies of Quantitatively Measured Skin, Hair, and Eye Pigmentation in Four European Populations. PloS One 7: e48294.

6. StokowskiRP, PantP, DaddT, FeredayA, HindsDA, et al. (2007) A genomewide association study of skin pigmentation in a South Asian population. Am J Hum Genet 81 : 1119–1132.

7. MillerCT, BelezaS, PollenAA, SchluterD, KittlesRA, et al. (2007) cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131 : 1179–1189.

8. JablonskiNG, ChaplinG (2000) The evolution of human skin coloration. J Hum Evol 39 : 57–106.

9. LoomisWF (1967) Skin-pigment regulation of vitamin-D biosynthesis in man. Science 157 : 501.

10. Robins AH (2005) Biological perspectives on human pigmentation. Cambridge University Press.

11. JuzenieneA, SetlowR, PorojnicuA, SteindalA, MoanJ (2009) Development of different human skin colors: a review highlighting photobiological and photobiophysical aspects. J Photochem Photobiol B 96 : 93.

12. MylesS, SomelM, TangK, KelsoJ, StonekingM (2007) Identifying genes underlying skin pigmentation differences among human populations. Hum Genet 120 : 613–621.

13. PickrellJK, CoopG, NovembreJ, KudaravalliS, LiJZ, et al. (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res 19 : 826–837.

14. NovembreJ, Di RienzoA (2009) Spatial patterns of variation due to natural selection in humans. Nat Rev Genet 10 : 745–755.

15. AnnoS, OhshimaK, AbeT (2010) Approaches to understanding adaptations of skin color variation by detecting geneenvironment interactions. Expert Rev Mol Diagn 10 : 987–991.

16. TangK, ThorntonKR, StonekingM (2007) A new approach for using genome scans to detect recent positive selection in the human genome. PLoS Biol 5: e171.

17. GingerRS, AskewSE, OgborneRM, WilsonS, FerdinandoD, et al. (2008) SLC24A5 encodes a trans-Golgi network protein with potassium-dependent sodium-calcium exchange activity that regulates human epidermal melanogenesis. J Biol Chem 283 : 5486.

18. TsetskhladzeZR, CanfieldVA, AngKC, WentzelSM, ReidKP, et al. (2012) Functional Assessment of Human Coding Mutations Affecting Skin Pigmentation Using Zebrafish. PloS One 7: e47398.

19. NortonHL, KittlesRA, ParraE, McKeigueP, MaoX, et al. (2007) Genetic evidence for the convergent evolution of light skin in Europeans and East Asians. Mol Biol Evol 24 : 710.

20. VoightBF, KudaravalliS, WenX, PritchardJK (2006) A map of recent positive selection in the human genome. PLoS Biol 4: e72.

21. SabetiPC, VarillyP, FryB, LohmuellerJ, HostetterE, et al. (2007) Genome-wide detection and characterization of positive selection in human populations. Nature 449 : 913–918.

22. JaswalI (1983) Pigmentary variation in Indian populations. Acta Anthropogenet 7 : 75.

23. PembertonTJ, MehtaNU, WitonskyD, Di RienzoA, AllayeeH, et al. (2008) Prevalence of common disease-associated variants in Asian Indians. BMC Genet 9 : 13.

24. MetspaluM, RomeroIG, YunusbayevB, ChaubeyG, MallickCB, et al. (2011) Shared and unique components of human population structure and genome-wide signals of positive selection in South Asia. Am J Hum Genet 89 : 731–744.

25. ReichD, ThangarajK, PattersonN, PriceAL, SinghL (2009) Reconstructing Indian population history. Nature 461 : 489–494.

26. ChaubeyG, MetspaluM, ChoiY, MägiR, RomeroIG, et al. (2011) Population genetic structure in Indian Austroasiatic speakers: the role of landscape barriers and sex-specific admixture. Mol Biol Evol 28 : 1013–1024.

27. YunusbayevB, MetspaluM, JärveM, KutuevI, RootsiS, et al. (2012) The Caucasus as an asymmetric semipermeable barrier to ancient human migrations. Mol Biol Evol 29 : 359–365.

28. BeharDM, YunusbayevB, MetspaluM, MetspaluE, RossetS, et al. (2010) The genome-wide structure of the Jewish people. Nature 466 : 238–242.

29. CoopG, PickrellJK, NovembreJ, KudaravalliS, LiJ, et al. (2009) The role of geography in human adaptation. PLoS Genet 5: e1000500.

30. IzagirreN, GarcíaI, JunqueraC, De La RúaC, AlonsoS (2006) A scan for signatures of positive selection in candidate loci for skin pigmentation in humans. Mol Biol Evol 23 : 1697.

31. De GruijterJM, LaoO, VermeulenM, XueY, WoodwarkC, et al. (2011) Contrasting signals of positive selection in genes involved in human skin-color variation from tests based on SNP scans and resequencing. Investig Genet 2 : 24.

32. NortonHL, KittlesRA, ParraE, McKeigueP, MaoX, et al. (2007) Genetic evidence for the convergent evolution of light skin in Europeans and East Asians. Mol Biol Evol 24 : 710.

33. AngKC, NguMS, ReidKP, TehMS, AidaZS, et al. (2012) Skin Color Variation in Orang Asli Tribes of Peninsular Malaysia. PloS One 7: e42752.

34. QuillenEE, BauchetM, BighamAW, Delgado-BurbanoME, FaustFX, et al. (2012) OPRM1 and EGFR contribute to skin pigmentation differences between Indigenous Americans and Europeans. Hum Genet 131 : 1073–1080.

35. BelezaS, JohnsonNA, CandilleSI, AbsherDM, CoramMA, et al. (2013) Genetic Architecture of Skin and Eye Color in an African-European Admixed Population. PLoS Genet 9: e1003372.

36. Sapovadia V (2012) Saurashtra: A Language, Region, Culture & Community. Available: http://papers.ssrn.com/sol3/papers.cfm?abstract_id=2033685.

37. ArunKumarG, Soria-HernanzDF, KavithaVJ, ArunVS, SyamaA, et al. (2012) Population differentiation of Southern Indian male lineages correlates with agricultural expansions predating the caste system. PloS One 7: e50269.

38. CordauxR, SahaN, BentleyGR, AungerR, SirajuddinS, et al. (2003) Mitochondrial DNA analysis reveals diverse histories of tribal populations from India. Eur J Hum Genet 11 : 253–264.

39. JablonskiNG (2004) The evolution of human skin and skin color. Annu Rev Anthr 33 : 585–623.

40. JablonskiNG, ChaplinG (2010) Human skin pigmentation as an adaptation to UV radiation. Proc Natl Acad Sci 107 : 8962–8968.

41. McEvoyB, BelezaS, ShriverMD (2006) The genetic architecture of normal variation in human pigmentation: an evolutionary perspective and model. Hum Mol Genet 15: R176–R181.

42. BelezaS, dos SantosAM, McEvoyB, AlvesI, MartinhoC, et al. (2012) The timing of pigmentation lightening in Europeans. Mol Biol Evol 30 (1) 24–35.

43. ScallyA, DurbinR (2012) Revising the human mutation rate: implications for understanding human evolution. Nat Rev Genet 13 : 745–753.

44. QuillenEE, ShriverMD (2011) Milestone 2. Nat Milestones E5–E7.

45. NortonHL, FriedlaenderJS, MerriwetherDA, KokiG, MgoneCS, et al. (2006) Skin and hair pigmentation variation in Island Melanesia. Am J Phys Anthropol 130 : 254–268.

46. ShriverMD, ParraEJ, DiosS, BonillaC, NortonH, et al. (2003) Skin pigmentation, biogeographical ancestry and admixture mapping. Hum Genet 112 : 387–399.

47. CannHM, de TomaC, CazesL, LegrandM-F, MorelV, et al. (2002) A human genome diversity cell line panel. Sci New York NY 296 : 261.

48. KuhnM (2008) Building predictive models in R using the caret package. J Stat Softw 28 : 1–26.

49. Rubin DB (1987) Multiple imputation for non-response in surveys. New York: John Wiley & Sons.

50. BuurenS, Groothuis-OudshoornK (2011) MICE: Multivariate imputation by chained equations in R. J Stat Softw 45.

51. ExcoffierL, LavalG, SchneiderS (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinforma Online 1 : 47.

52. AlexanderDH, NovembreJ, LangeK (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19 : 1655–1664.

53. LibradoP, RozasJ (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 : 1451–1452.

54. TajimaF (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 : 585–595.

55. FuY-X, LiW-H (1993) Statistical tests of neutrality of mutations. Genetics 133 : 693–709.

56. SchaffnerSF, FooC, GabrielS, ReichD, DalyMJ, et al. (2005) Calibrating a coalescent simulation of human genome sequence variation. Genome Res 15 : 1576–1583.

57. FrazerKA, BallingerDG, CoxDR, HindsDA, StuveLL, et al. (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449 : 851–861.

58. BrowningSR, BrowningBL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81 : 1084.

59. StephensM, DonnellyP (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73 : 1162–1169.

60. TamuraK, PetersonD, PetersonN, StecherG, NeiM, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28 : 2731–2739.

61. BarrettJ, FryB, MallerJ, DalyM (2005) Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21 : 263–265.

62. DrummondAJ, RambautA (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7 : 214.

63. FelsensteinJ (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17 : 368–376.

64. KeaneTM, CreeveyCJ, PentonyMM, NaughtonTJ, MclnerneyJO (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6 : 29.

65. MininVN, BloomquistEW, SuchardMA (2008) Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol Biol Evol 25 : 1459–1471.

66. Rambaut A, Drummond A (2007) Tracer version 1.5. Available: http://beast. bio. ed. ac. uk.

67. ForsterP, HardingR, TorroniA, BandeltH-J (1996) Origin and evolution of Native American mtDNA variation: a reappraisal. Am J Hum Genet 59 : 935.

68. SaillardJ, ForsterP, LynnerupN, BandeltH-J, NørbyS (2000) mtDNA Variation among Greenland Eskimos: The Edge of theBeringian Expansion. Am J Hum Genet 67 : 718.

69. ParraEJ, KittlesRA, ShriverMD (2004) Implications of correlations between skin color and genetic ancestry for biomedical research. Nat Genet 36: S54–S60.

70. ShriverMD, ParraEJ (2000) Comparison of narrow-band reflectance spectroscopy and tristimulus colorimetry for measurements of skin and hair color in persons of different biological ancestry. Am J Phys Anthropol 112 : 17.