Native American admixture recapitulates population-specific migration and settlement of the continental United States

English version

Autoři: I. King Jordan ^aff001; Lavanya Rishishwar ^aff002; Andrew B. Conley ^aff001
Působiště autorů: School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, United States of America ^aff001; IHRC-Georgia Tech Applied Bioinformatics Laboratory, Atlanta, Georgia, United States of America ^aff002; PanAmerican Bioinformatics Institute, Cali, Valle del Cauca, Colombia ^aff003
Vyšlo v časopise: Native American admixture recapitulates population-specific migration and settlement of the continental United States. PLoS Genet 15(9): e32767. doi:10.1371/journal.pgen.1008225
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008225

Souhrn

European and African descendants settled the continental US during the 17^th-19^th centuries, coming into contact with established Native American populations. The resulting admixture among these groups yielded a significant reservoir of Native American ancestry in the modern US population. We analyzed the patterns of Native American admixture seen for the three largest genetic ancestry groups in the US population: African descendants, Western European descendants, and Spanish descendants. The three groups show distinct Native American ancestry profiles, which are indicative of their historical patterns of migration and settlement across the country. Native American ancestry in the modern African descendant population does not coincide with local geography, instead forming a single group with origins in the southeastern US, consistent with the Great Migration of the early 20^th century. Western European descendants show Native American ancestry that tracks their geographic origins across the US, indicative of ongoing contact during westward expansion, and Native American ancestry can resolve Spanish descendant individuals into distinct local groups formed by more recent migration from Mexico and Puerto Rico. We found an anomalous pattern of Native American ancestry from the US southwest, which most likely corresponds to the Nuevomexicano descendants of early Spanish settlers to the region. We addressed a number of controversies surrounding this population, including the extent of Sephardic Jewish ancestry. Nuevomexicanos are less admixed than nearby Mexican-American individuals, with more European and less Native American and African ancestry, and while they do show demonstrable Sephardic Jewish ancestry, the fraction is no greater than seen for other New World Spanish descendant populations.

Klíčová slova:

Census – Comparative genomics – Europe – Haplotypes – Mexican people – Population genetics – United States – Native American people

Zdroje

1. Reich D. Who We Are and How We Got Here: Ancient DNA and the new science of the human past: Oxford University Press; 2018.

2. Reich D, Patterson N, Campbell D, Tandon A, Mazieres S, Ray N, et al. Reconstructing Native American population history. Nature. 2012;488(7411):370–4. doi: 10.1038/nature11258 22801491.

3. Jenkins DL, Davis LG, Stafford TW Jr., Campos PF, Hockett B, Jones GT, et al. Clovis age Western Stemmed projectile points and human coprolites at the Paisley Caves. Science. 2012;337(6091):223–8. doi: 10.1126/science.1218443 22798611.

4. Fuson RH. Juan Ponce de León and the Spanish Discovery of Puerto Rico and Florida: McDonald and Woodward Publishing Company; 2000.

5. Price DA. Love and hate in Jamestown: John Smith, Pocahontas, and the start of a new nation: Vintage; 2007.

6. Hashaw T. The birth of Black America: The first African Americans and the pursuit of freedom at Jamestown: Basic Books; 2007.

7. Eltis D, Richardson D. Atlas of the Transatlantic Slave Trade: Yale University Press; 2010.

8. Mann CC. 1491: New revelations of the Americas before Columbus: Alfred a Knopf Incorporated; 2005.

9. Mann CC. 1493: uncovering the new world Columbus created. 1st ed. New York N.Y.: Alfred A. Knopf; 2011. xix, 535 pages p.

10. Hellenthal G, Busby GBJ, Band G, Wilson JF, Capelli C, Falush D, et al. A genetic atlas of human admixture history. Science. 2014;343(6172):747–51. doi: 10.1126/science.1243518 24531965.

11. Goldberg A, Rosenberg NA. Beyond 2/3 and 1/3: The Complex Signatures of Sex-Biased Admixture on the X Chromosome. Genetics. 2015;201(1):263–79. doi: 10.1534/genetics.115.178509 26209245.

12. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, Ramachandran S, et al. Worldwide human relationships inferred from genome-wide patterns of variation. Science. 2008;319(5866):1100–4. doi: 10.1126/science.1153717 18292342.

13. Patterson N, Moorjani P, Luo Y, Mallick S, Rohland N, Zhan Y, et al. Ancient admixture in human history. Genetics. 2012;192(3):1065–93. Epub 2012/09/11. doi: 10.1534/genetics.112.145037 22960212.

14. Gonzales PB. Whither the Nuevomexicanos: The career of a southwestern intellectual discourse, 1907–2004. Soc Sci J. 2006;43(2):273–86. doi: 10.1016/j.soscij.2006.02.006

15. Healy ME, Hill D, Berwick M, Edgar H, Gross J, Hunley K. Social-group identity and population substructure in admixed populations in New Mexico and Latin America. PLoS One. 2017;12(10):e0185503. doi: 10.1371/journal.pone.0185503 28977000.

16. Hordes SM. To the end of the earth: a history of the crypto-Jews of New Mexico: Columbia University Press; 2008.

17. Chacon-Duque JC, Adhikari K, Fuentes-Guajardo M, Mendoza-Revilla J, Acuna-Alonzo V, Lozano RB, et al. Latin Americans show wide-spread Converso ancestry and the imprint of local Native ancestry on physical appearance. bioRxiv. 2018:252155.

18. Wilkerson I. The warmth of other suns: The epic story of America’s great migration: Vintage; 2011.

19. Baharian S, Barakatt M, Gignoux CR, Shringarpure S, Errington J, Blot WJ, et al. The Great Migration and African-American Genomic Diversity. PLoS Genet. 2016;12(5):e1006059. doi: 10.1371/journal.pgen.1006059 27232753.

20. Pascoe P. What comes naturally: Miscegenation law and the making of race in America: Oxford University Press on Demand; 2009.

21. Bryc K, Velez C, Karafet T, Moreno-Estrada A, Reynolds A, Auton A, et al. Colloquium paper: genome-wide patterns of population structure and admixture among Hispanic/Latino populations. Proc Natl Acad Sci U S A. 2010;107 Suppl 2:8954–61. 20445096.

22. Rishishwar L, Conley AB, Wigington CH, Wang L, Valderrama-Aguirre A, Jordan IK. Ancestry, admixture and fitness in Colombian genomes. Sci Rep. 2015;5:12376. doi: 10.1038/srep12376 26197429.

23. Bryc K, Auton A, Nelson MR, Oksenberg JR, Hauser SL, Williams S, et al. Genome-wide patterns of population structure and admixture in West Africans and African Americans. Proc Natl Acad Sci U S A. 2010;107(2):786–91. doi: 10.1073/pnas.0909559107 20080753.

24. Lind JM, Hutcheson-Dilks HB, Williams SM, Moore JH, Essex M, Ruiz-Pesini E, et al. Elevated male European and female African contributions to the genomes of African American individuals. Hum Genet. 2007;120(5):713–22. doi: 10.1007/s00439-006-0261-7 17006671.

25. TallBear K. Native American DNA: Tribal belonging and the false promise of genetic science: University of Minnesota Press; 2013.

26. Nieto-Phillips JM. The language of blood: The making of Spanish-American identity in New Mexico, 1880s-1930s: UNM Press; 2008.

27. Wade P. Race and sex in Latin America. New York: Pluto Press; 2009.

28. Vasconcelos J. La raza cósmica: misión de la raza iberoamericana: Agencia Mundial de Librería; 1925.

29. Moreno-Estrada A, Gravel S, Zakharia F, McCauley JL, Byrnes JK, Gignoux CR, et al. Reconstructing the population genetic history of the Caribbean. PLoS Genet. 2013;9(11):e1003925. doi: 10.1371/journal.pgen.1003925 24244192 Ancestry.com, 23andMe’s "Roots into the Future" project, and Personalis, Inc. He is on the medical advisory board of Invitae and Med-tek. None of these entities played any role in the project or research results reported here.

30. Conley AB, Rishishwar L, Norris ET, Valderrama-Aguirre A, Marino-Ramirez L, Medina-Rivas MA, et al. A Comparative Analysis of Genetic Ancestry and Admixture in the Colombian Populations of Choco and Medellin. G3 (Bethesda). 2017;7(10):3435–47. doi: 10.1534/g3.117.1118 28855283.

31. Moreno-Estrada A, Gignoux CR, Fernandez-Lopez JC, Zakharia F, Sikora M, Contreras AV, et al. Human genetics. The genetics of Mexico recapitulates Native American substructure and affects biomedical traits. Science. 2014;344(6189):1280–5. doi: 10.1126/science.1251688 24926019.

32. Gravel S. Population genetics models of local ancestry. Genetics. 2012;191(2):607–19. Epub 2012/04/12. doi: 10.1534/genetics.112.139808 22491189.

33. Homburger JR, Moreno-Estrada A, Gignoux CR, Nelson D, Sanchez E, Ortiz-Tello P, et al. Genomic Insights into the Ancestry and Demographic History of South America. PLoS Genet. 2015;11(12):e1005602. Epub 2015/12/05. doi: 10.1371/journal.pgen.1005602 26636962.

34. Roth N. Conversos, Inquisition, and the Expulsion of the Jews from Spain: Univ of Wisconsin Press; 2002.

35. Ferry B, Nathan D. Mistaken Identity? The Case of New Mexico’s’ Hidden Jews’. Atlantic Monthly. 2000;283(6):85–96.

36. Weitz JS. Let my people go (home) to Spain: a genealogical model of Jewish identities since 1492. PLoS One. 2014;9(1):e85673. doi: 10.1371/journal.pone.0085673 24465647.

37. Genomes Project C, Abecasis GR, Altshuler D, Auton A, Brooks LD, Durbin RM, et al. A map of human genome variation from population-scale sequencing. Nature. 2010;467(7319):1061–73. doi: 10.1038/nature09534 20981092.

38. Genomes Project C, Auton A, Brooks LD, Durbin RM, Garrison EP, Kang HM, et al. A global reference for human genetic variation. Nature. 2015;526(7571):68–74. doi: 10.1038/nature15393 26432245.

39. Cann HM, de Toma C, Cazes L, Legrand MF, Morel V, Piouffre L, et al. A human genome diversity cell line panel. Science. 2002;296(5566):261–2. doi: 10.1126/science.296.5566.261b 11954565.

40. Jakobsson M, Scholz SW, Scheet P, Gibbs JR, VanLiere JM, Fung HC, et al. Genotype, haplotype and copy-number variation in worldwide human populations. Nature. 2008;451(7181):998–1003. doi: 10.1038/nature06742 18288195.

41. Behar DM, Yunusbayev B, Metspalu M, Metspalu E, Rosset S, Parik J, et al. The genome-wide structure of the Jewish people. Nature. 2010;466(7303):238–42. doi: 10.1038/nature09103 20531471.

42. Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ. Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience. 2015;4:7. doi: 10.1186/s13742-015-0047-8 25722852.

43. Team RC. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. 2017.

44. Delaneau O, Zagury JF, Marchini J. Improved whole-chromosome phasing for disease and population genetic studies. Nature methods. 2013;10(1):5–6. doi: 10.1038/nmeth.2307 23269371.

45. Maples BK, Gravel S, Kenny EE, Bustamante CD. RFMix: a discriminative modeling approach for rapid and robust local-ancestry inference. Am J Hum Genet. 2013;93(2):278–88. doi: 10.1016/j.ajhg.2013.06.020 23910464.

46. Fortes-Lima C, Gessain A, Ruiz-Linares A, Bortolini MC, Migot-Nabias F, Bellis G, et al. Genome-wide Ancestry and Demographic History of African-Descendant Maroon Communities from French Guiana and Suriname. Am J Hum Genet. 2017;101(5):725–36. doi: 10.1016/j.ajhg.2017.09.021 29100086.

47. Alexander DH, Novembre J, Lange K. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 2009;19(9):1655–64. doi: 10.1101/gr.094052.109 19648217.

48. Meyer D, Dimitriadou E, Hornik K, Weingessel A, Leisch F. e1071: Misc Functions of the Department of Statistics (e1071), TU Wien, 2014. R package version. 2015:1.6–4.

49. Patterson N, Price AL, Reich D. Population structure and eigenanalysis. PLoS Genet. 2006;2(12):e190. Epub 2006/12/30. doi: 10.1371/journal.pgen.0020190 17194218.

50. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4(4):406–25. doi: 10.1093/oxfordjournals.molbev.a040454 3447015.

51. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9. doi: 10.1093/molbev/mst197 24132122.

52. Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004;20(2):289–90. Epub 2004/01/22. doi: 10.1093/bioinformatics/btg412 14734327.