Reconstructing Native American Migrations from Whole-Genome and Whole-Exome Data

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There is great scientific and popular interest in understanding the genetic history of populations in the Americas. We wish to understand when different regions of the continent were inhabited, where settlers came from, and how current inhabitants relate genetically to earlier populations. Recent studies unraveled parts of the genetic history of the continent using genotyping arrays and uniparental markers. The 1000 Genomes Project provides a unique opportunity for improving our understanding of population genetic history by providing over a hundred sequenced low coverage genomes and exomes from Colombian (CLM), Mexican-American (MXL), and Puerto Rican (PUR) populations. Here, we explore the genomic contributions of African, European, and especially Native American ancestry to these populations. Estimated Native American ancestry is in MXL, in CLM, and in PUR. Native American ancestry in PUR is most closely related to populations surrounding the Orinoco River basin, confirming the Southern America ancestry of the Taíno people of the Caribbean. We present new methods to estimate the allele frequencies in the Native American fraction of the populations, and model their distribution using a demographic model for three ancestral Native American populations. These ancestral populations likely split in close succession: the most likely scenario, based on a peopling of the Americas thousand years ago (kya), supports that the MXL Ancestors split kya, with a subsequent split of the ancestors to CLM and PUR kya. The model also features effective populations of in Mexico, in Colombia, and in Puerto Rico. Modeling Identity-by-descent (IBD) and ancestry tract length, we show that post-contact populations also differ markedly in their effective sizes and migration patterns, with Puerto Rico showing the smallest effective size and the earlier migration from Europe. Finally, we compare IBD and ancestry assignments to find evidence for relatedness among European founders to the three populations.

Vyšlo v časopise: Reconstructing Native American Migrations from Whole-Genome and Whole-Exome Data. PLoS Genet 9(12): e32767. doi:10.1371/journal.pgen.1004023
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004023

Souhrn

Zdroje

1. Genomes Project Consortium (2012) An integrated map of genetic variation from 1,092 human genomes. Nature 491: 56–65.

2. O'RourkeDH, RaffJA (2010) The human genetic history of the Americas: the final frontier. Curr Biol 20: R202–R207.

3. Luis LanataJ, MartinoL, OsellaA, Garcia-HerbstA (2008) Demographic conditions necessary to colonize new spaces: the case for early human dispersal in the Americas. World Archaeology 40: 520–537.

4. GoebelT, WatersMR, O'RourkeDH (2008) The late Pleistocene dispersal of modern humans in the Americas. Science 319: 1497–1502.

5. DillehayTD (2009) Probing deeper into first American studies. Proc Natl Acad Sci USA 106: 971–978.

6. DillehayTD, RamrezC, PinoM, CollinsMB, RossenJ, et al. (2008) Monte Verde: seaweed, food, medicine, and the peopling of South America. Science 320: 784–786.

7. BodnerM, PeregoUA, HuberG, FendtL, RockAW, et al. (2012) Rapid coastal spread of First Americans: Novel insights from South America's Southern Cone mitochondrial genomes. Genome Res 22: 811–820.

8. HurstCT (1943) A Folsom site in a mountain valley of Colorado. American Antiquity 8: 250–253.

9. Meltzer DJ (2009) First Peoples in a New World. Colonizing Ice Age America. Univ of California Press.

10. Rouse I (1992) The Tainos: Rise and decline of the people who greeted Columbus. Yale University Press.

11. Rodrguez-Ramos R (2010) Rethinking Puerto Rican Precolonial History. University Alabama Press.

12. Veloz Maggiolo M (1991) Panorama histórico del caribe precolombino. Quinto Centenario del Descubrimiento de América Banco Central de la República Dominicana.

13. HopperR (2008) Taino Indians: Settlements of the Caribbean. Lambda Alpha Journal 38: 62–69.

14. Moscoso F (2008) Caciques, aldeas y población tana de Boriquén (Puerto Rico), 1492–1582. Academia Puertorriqueña de la Historia.

15. Alegra RE, Quiñones ER (1999) Historia y cultura de Puerto Rico: Desde la época pre-colombina hasta nuestros das. Fundación Francisco Carvajal.

16. ViaM, GignouxCR, RothLA, FejermanL, GalanterJ, et al. (2011) History Shaped the Geographic Distribution of Genomic Admixture on the Island of Puerto Rico. PLoS ONE 6: e16513.

17. UnderhillPA, JinL, ZemansR, OefnerPJ, Cavalli-SforzaLL (1996) A pre-Columbian Y chromosome-specific transition and its implications for human evolutionary history. Proc Natl Acad Sci USA 93: 196–200.

18. LellJT, BrownMD, SchurrTG, SukernikRI, StarikovskayaYB, et al. (1997) Y chromosome polymorphisms in native American and Siberian populations: identification of native American Y chromosome haplotypes. Hum Genet 100: 536–543.

19. BianchiNO, CatanesiCI, BaillietG, Martinez-MarignacVL, BraviCM, et al. (1998) Characterization of ancestral and derived Y-chromosome haplotypes of New World native populations. Am J Hum Genet 63: 1862–1871.

20. KarafetTM, ZeguraSL, PosukhO, OsipovaL, BergenA, et al. (1999) Ancestral Asian source(s) of new world Y-chromosome founder haplotypes. Am J Hum Genet 64: 817–831.

21. BortoliniMC, SalzanoFM, ThomasMG, StuartS, NasanenSPK, et al. (2003) Y-chromosome evidence for differing ancient demographic histories in the Americas. Am J Hum Genet 73: 524–539.

22. MesaNR, MondragónMC, SotoID, ParraMV, DuqueC, et al. (2000) Autosomal, mtDNA, and Y-chromosome diversity in Amerinds: pre- and post-Columbian patterns of gene flow in South America. Am J Hum Genet 67: 1277–1286.

23. BortoliniMC, SalzanoFM, BauCHD, LayrisseZ, Petzl-ErlerML, et al. (2002) Y-chromosome biallelic polymorphisms and Native American population structure. Ann Hum Genet 66: 255–259.

24. BaillietG, RamalloV, MuzzioM, GarcíaA, SantosMR, et al. (2009) Brief communication: Restricted geographic distribution for Y-Q* paragroup in South America. Am J Phys Anthropol 140: 578–582.

25. TorroniA, SchurrTG, CabellMF, BrownMD, NeelJV, et al. (1993) Asian affinities and continental radiation of the four founding Native American mtDNAs. Am J Hum Genet 53: 563–590.

26. AchilliA, PeregoUA, BraviCM, CobleMD, KongQP, et al. (2008) The Phylogeny of the Four Pan-American MtDNA Haplogroups: Implications for Evolutionary and Disease Studies. PLoS ONE 3: e1764.

27. KumarS, BellisC, ZlojutroM, MeltonPE, BlangeroJ, et al. (2011) Large scale mitochondrial sequencing in Mexican Americans suggests a reappraisal of Native American origins. BMC Evol Biol 11: 293.

28. MalhiRS, CybulskiJS, TitoRY, JohnsonJ, HarryH, et al. (2010) Brief communication: mitochondrial haplotype C4c confirmed as a founding genome in the Americas. Am J Phys Anthropol 141: 494–497.

29. PeregoUA, AchilliA, AngerhoferN, AccetturoM, PalaM, et al. (2009) Distinctive Paleo-Indian migration routes from Beringia marked by two rare mtDNA haplogroups. Curr Biol 19: 1–8.

30. PeregoUA, AngerhoferN, PalaM, OlivieriA, LancioniH, et al. (2010) The initial peopling of the Americas: a growing number of founding mitochondrial genomes from Beringia. Genome Res 20: 1174–1179.

31. TammE, KivisildT, ReidlaM, MetspaluM, SmithDG, et al. (2007) Beringian standstill and spread of Native American founders. PLoS ONE 2: e829.

32. SandovalK, Buentello-MaloL, Peñaloza-EspinosaR, AvelinoH, SalasA, et al. (2009) Linguistic and maternal genetic diversity are not correlated in Native Mexicans. Hum Genet 126: 521–531.

33. BonattoSL, SalzanoFM (1997) A single and early migration for the peopling of the Americas supported by mitochondrial DNA sequence data. Proc Natl Acad Sci USA 94: 1866–1871.

34. MulliganCJ, KitchenA, MiyamotoMM (2008) Updated three-stage model for the peopling of the Americas. PLoS ONE 3: e3199.

35. FagundesNJR, KanitzR, EckertR, VallsACS, BogoMR, 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.

36. WangS, LewisCM, JakobssonM, RamachandranS, RayN, et al. (2007) Genetic variation and population structure in native Americans. PLoS Genet 3: e185.

37. RojasW, ParraMV, CampoO, CaroMA, LoperaJG, et al. (2010) Genetic make up and structure of Colombian populations by means of uniparental and biparental DNA markers. Am J Phys Anthropol 143: 13–20.

38. YangNN, MazieresS, BraviC, RayN, WangS, et al. (2010) Contrasting patterns of nuclear and mtDNA diversity in Native American populations. Ann Hum Genet 74: 525–538.

39. ScliarMO, Soares-SouzaGB, ChevitareseJ, LemosL, MagalhãesWCS, et al. (2012) The population genetics of quechuas, the largest native south american group: Autosomal sequences, SNPs, and microsatellites evidence high level of diversity. Am J Phys Anthropol 147: 443–451.

40. ReichD, PattersonN, CampbellD, TandonA, MazieresS, et al. (2012) Reconstructing Native American population history. Nature 488: 370–374.

41. Martínez-CortésG, Salazar-FloresJ, Fernández-RodríguezLG, Rubi-CastellanosR, Rodrguez-LoyaC, et al. (2012) Admixture and population structure in Mexican-Mestizos based on paternal lineages. J Hum Genet 57: 568–574.

42. Rubi-CastellanosR, Martínez-CortésG, Muñoz-ValleJF, González-MartínA, Cerda-FloresRM, et al. (2009) Pre-Hispanic Mesoamerican demography approximates the present-day ancestry of Mestizos throughout the territory of Mexico. Am J Phys Anthropol 139: 284–294.

43. BedoyaG, MontoyaP, GarcíaJ, SotoI, BourgeoisS, et al. (2006) Admixture dynamics in Hispanics: a shift in the nuclear genetic ancestry of a South American population isolate. Proc Natl Acad Sci USA 103: 7234–7239.

44. Martínez-CruzadoJC, Toro-LabradorG, Viera-VeraJ, Rivera-VegaMY, StartekJ, et al. (2005) Reconstructing the population history of Puerto Rico by means of mtDNA phylogeographic analysis. Am J Phys Anthropol 128: 131–155.

45. BolnickDA, BolnickDI, SmithDG (2006) Asymmetric male and female genetic histories among Native Americans from Eastern North America. Mol Biol Evol 23: 2161–2174.

46. Carvajal-CarmonaLG, SotoID, PinedaN, Ortíz-BarrientosD, DuqueC, et al. (2000) Strong Amerind/White Sex Bias and a Possible Sephardic Contribution among the Founders of a Population in Northwest Colombia. The American Journal of Human Genetics 67: 1287–1295.

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

48. MaplesBK, GravelS, KennyEE, BustamanteCD (2013) RFMix: A Discriminative Modeling Approach for Rapid and Robust Local-Ancestry Inference. Am J Hum Genet 93: 278–288.

49. GalanterJM, Fernandez-LopezJC, GignouxCR, Barnholtz-SloanJ, Fernandez-RozadillaC, et al. (2012) Development of a panel of genome-wide ancestry informative markers to study admixture throughout the Americas. PLoS Genet 8: e1002554.

50. Moreno-EstradaA, GravelS, ZakhariaF, McCauleyJL, ByrnesJK, et al. (2013) Reconstructing the Population Genetic History of the Caribbean. arXiv

51. MoseleyC (2004) Encyclopedia of the World's Endangered Languages. Routledge

52. CombesI, LowreyK (2006) Slaves without Masters? Arawakan Dynasties among the Chiriguano (Bolivian Chaco, Sixteenth to Twentieth Centuries). Ethnohistory 53: 689–714.

53. GravelS (2012) Population genetics models of local ancestry. Genetics 191: 607–619.

54. KiddJM, GravelS, ByrnesJ, Moreno-EstradaA, MusharoffS, et al. (2012) Population genetic inference from personal genome data: impact of ancestry and admixture on human genomic variation. Am J Hum Genet 91: 660–671.

55. GusevA, LoweJK, StoffelM, DalyMJ, AltshulerD, et al. (2008) Whole population, genome-wide mapping of hidden relatedness. Genome Res 19: 318–326.

56. PalamaraPF, LenczT, DarvasiA, Pe'erI (2012) Length distributions of identity by descent reveal fine-scale demographic history. Am J Hum Genet 91: 809–822.

57. BaranY, PasaniucB, SankararamanS, TorgersonDG, GignouxC, et al. (2012) Fast and accurate inference of local ancestry in Latino populations. Bioinformatics 28: 1359–1367.

58. GutenkunstRN, HernandezRD, WilliamsonSH, BustamanteCD (2009) Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet 5: e1000695.

59. MyersS, FeffermanC, PattersonN (2008) Can one learn history from the allelic spectrum? Theor Popul Biol 73: 342–348.

60. Salzano FM, Bortolini MC (2005) The Evolution and Genetics of Latin American Populations. Cambridge University Press.

61. Moscoso F (2008) Caciques, aldeas y población taína de Boriquén (Puerto Rico), 1492–1582. Academia puertorriquena de la historia.

62. DobynsHF (1966) An appraisal of techniques with a new hemispheric estimate. Current Anthropology 7: 395–416.

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

64. SandersSJ, MurthaMT, GuptaAR, MurdochJD, RaubesonMJ, et al. (2012) De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature 485: 237–241.

65. GorostizaA, Acunha-AlonzoV, Regalado-LiuL, TiradoS, GranadosJ, et al. (2012) Reconstructing the history of Mesoamerican populations through the study of the mitochondrial DNA control region. PLoS ONE 7: e44666.

66. BrycK, VelezC, KarafetT, Moreno-EstradaA, ReynoldsA, et al. (2010) Colloquium paper: genome-wide patterns of population structure and admixture among Hispanic/Latino populations. Proc Natl Acad Sci USA 107 Suppl 2: 8954–8961.

67. WangS, RayN, RojasW, ParraMV, BedoyaG, et al. (2008) Geographic patterns of genome admixture in Latin American Mestizos. PLoS Genet 4: e1000037.

68. TremblayM, VézinaH (2000) New estimates of intergenerational time intervals for the calculation of age and origins of mutations. Am J Hum Genet 66: 651–658.