Arrival of Paleo-Indians to the Southern Cone of South America: New Clues from Mitogenomes

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  de Saint Pierre, Michelle ^a,b   Gandini, Francesca ^c   Perego, Ugo A ^c,d   Bodner, Martin ^e   Gómez Carballa, Alberto ^f   Corach, Daniel ^g   Angerhofer, Norman ^d,h   Woodward, Scott R ^d,h   Semino, Ornella ^c   Salas, Antonio ^f   Parson, Walther ^e,i   Moraga, Mauricio ^a,b   Achilli, Alessandro ^j   Torroni, Antonio ^c   Olivieri, Anna ^c  

^a UNIVERSITY OF CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

^c UNIVERSITY OF PAVIA   (Italy)

^d Sorenson Molecular Genealogy Foundation   (United States)

^e INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^f UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^g UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^h Ancestry   (United States)

ⁱ PENNSYLVANIA STATE UNIVERSITY   (United States)

^j UNIVERSITY OF PERUGIA   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

AMINO ACID SUBSTITUTION; ARGENTINA; ARTICLE; CHILE; CLADISTICS; EVOLUTIONARY ADAPTATION; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GEOGRAPHIC DISTRIBUTION; GEOGRAPHIC ORIGIN; HUMAN; MITOCHONDRIAL GENOME; MOLECULAR PHYLOGENY; NUCLEOTIDE SEQUENCE; PHYLOGEOGRAPHY; POPULATION GENETICS;

ASIAN CONTINENTAL ANCESTRY GROUP; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; FEMALE; GENOME, MITOCHONDRIAL; HAPLOTYPES; HUMANS; INDIANS, NORTH AMERICAN; PHYLOGENY; SOUTH AMERICA;

EID: 84871167089     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051311     Document Type: Article

References (82)

1. Greenberg JH, Turner CGII, Zegura SL, (1986) The settlement of the Americas: a comparison of the linguistic, dental and genetic evidence. Curr Anthropol 27: 477-497.
2. Goebel T, Waters MR, ORourke DH, (2008) The late Pleistocene dispersal of modern humans in the Americas. Science 319: 1497-1502.
3. Schurr TG, (2004) The peopling of the newworld: perspectives from molecular anthropology. Annu Rev Anthropol 33: 551-583.
4. ORourke DH, Raff JA, (2010) The human genetic history of the Americas: the final frontier. Curr Biol 20: R202-7.
5. Dillehay TD, Ramírez C, Pino M, Collins MB, Rossen J, et al. (2008) Monte Verde: seaweed, food, medicine, and the peopling of South America. Science 320: 784-786.
6. Erlandson JM, Braje TJ, Graham MH, (2008) How old is MVII? Seaweeds, shorelines, and the pre-Clovis chronology at Monte Verde, Chile. J Isl & Coast Archaeol 3: 277-281.
7. Waters MR, Forman SL, Jennings TA, Nordt LC, Driese SG, et al. (2011) The Buttermilk Creek complex and the origins of Clovis at the Debra L. Friedkin site, Texas. Science 331: 1599-1603.
8. Curry A, (2012) Ancient migration: Coming to America. Nature 485: 30-32.
9. Kemp BM, Malhi RS, McDonough J, Bolnick DA, Eshleman JA, et al. (2007) Genetic analysis of early Holocene skeletal remains from Alaska and its implications for the settlement of the Americas. Am J Phys Anthropol 132: 605-621.
10. Gilbert T, Jenkins DL, Gotherstrom A, Naveran N, Sanchez JJ, et al. (2008) DNA from Pre-Clovis human coprolites in Oregon, North America. Science 320: 786-789.
11. Gilbert MT, Kivisild T, Grønnow B, Andersen PK, Metspalu E, et al. (2008) Paleo-Eskimo mtDNA genome reveals matrilineal discontinuity in Greenland. Science 320: 1787-1789.
12. Raff J, Tackney J, ORourke D, (2010) South from Alaska: a pilot aDNA study of genetic history on the Alaska Peninsula and the Eastern Aleutians. Hum Biol 82: 677-693.
13. Fagundes N, Kanitz R, Bonatto SL, (2008) A reevaluation of the Native American mtDNA genome diversity and its bearing on the models of early colonization of Beringia. PLoS One 3: e3157.
14. Tamm E, Kivisild T, Reidla M, Metspalu M, Glenn-Smith D, et al. (2007) Beringian standstill and spread of Native American founders. PLoS One 2: 1-6.
15. Ray N, Wegmann D, Fagundes NJR, Wang S, Ruiz-Linares A, et al. (2010) A statistical evaluation of models for the initial settlement of the American continent emphasizes the importance of gene flow with Asia. Mol Biol Evol 27: 337-345.
16. Kumar S, Bellis C, Zlojutro M, Melton PE, Blangero J, et al. (2011) Large scale mitochondrial sequencing in Mexican Americans suggests a reappraisal of Native American origins. BMC Evol Biol 11: 293.
17. Bodner M, Perego UA, Huber G, Fendt L, Röck AW, et al. (2012) Rapid coastal spread of First Americans: novel insights from South America's Southern Cone mitochondrial genomes. Genome Res 22: 811-820.
18. Fix AG, (2005) Rapid deployment of the five founding Amerind mtDNA haplogroups via coastal and riverine colonization. Am J Phys Anthropol 128: 430-436.
19. Fagundes N, Kanitz R, Eckert R, Valls ACS, Bogo MR, 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.
20. Kemp BM, González-Oliver A, Malhi RS, Monroe C, Schroeder KB, et al. (2010) Evaluating the farming/language dispersal hypothesis with genetic variation exhibited by populations in the Southwest and Mesoamerica. Proc Natl Acad Sci U S A 107: 6759-6764.
21. Perego UA, Achilli A, Angerhofer N, Accetturo M, Pala M, et al. (2009) Distinctive Paleo-Indian migration routes from Beringia marked by two rare mtDNA haplogroups. Curr Biol 19: 1-8.
22. Perego UA, Angerhofer N, Pala M, Olivieri A, Lancioni H, et al. (2010) The initial peopling of the Americas: a growing number of founding mitochondrial genomes from Beringia. Genome Res 20: 1174-1179.
23. Hooshiar Kashani B, Perego UA, Olivieri A, Angerhofer N, Gandini F, et al. (2012) Mitochondrial haplogroup C4c: a rare lineage entering America through the ice-free corridor? Am J Phys Anthropol 147: 35-39.
24. Behar DM, van Oven M, Rosset S, Metspalu M, Loogväli EL, et al. (2012) A "Copernican" reassessment of the human mitochondrial DNA tree from its root. Am J Hum Genet 90: 675-684.
25. Schurr TG, Ballinger SW, Gan YY, Hodge JA, Merriwether DA, et al. (1990) Amerindian mitochondrial DNAs have rare Asian mutations at high frequencies, suggesting they derived from four primary maternal lineages. Am J Hum Genet 46: 613-623.
26. Torroni A, Schurr TG, Yang CC, Szathmary EJ, Williams RC, et al. (1992) Native American mitochondrial DNA analysis indicates that the Amerind and the Nadene populations were founded by two independent migrations. Genetics 130: 153-162.
27. Torroni A, Schurr TG, Cabell MF, Brown MD, Neel JV, et al. (1993) Asian affinities and continental radiation of the four founding Native American mtDNAs. Am J Hum Genet 53: 563-590.
28. Bandelt HJ, Herrnstadt C, Yao YG, Kong QP, Kivisild T, et al. (2003) Identification of Native American founder mtDNAs through the analysis of complete mtDNA sequences: some caveats. Ann Hum Genet 67: 512-524.
29. Schurr TG, Sherry ST, (2004) Mitochondrial DNA and Y chromosome diversity and the peopling of the Americas: evolutionary and demographic evidence. Am J Hum Biol 16: 420-439.
30. Brown MD, Hosseini SH, Torroni A, Bandelt HJ, Allen JC, et al. (1998) MtDNA haplogroup X: an ancient link between Europe/Western Asia and North America? Am J Hum Genet 63: 1852-1861.
31. Malhi RS, Mortensen HM, Eshleman JA, Kemp BM, Lorenz JG, et al. (2003) Native American mtDNA prehistory in the American Southwest. Am J Phys Anthropol 120: 108-124.
32. Helgason A, Pálsson G, Pedersen HS, Angulalik E, Gunnarsdóttir ED, et al. (2006) mtDNA variation in Inuit populations of Greenland and Canada: migration history and population structure. Am J Phys Anthropol 130: 123-134.
33. Achilli A, Perego UA, Bravi CM, Coble MD, Kong QP, et al. (2008) The phylogeny of the four pan-American mtDNA haplogroups: implications for evolutionary and disease studies. PLoS One 3: e1764.
34. Malhi RS, Cybulski JS, Tito RY, Johnson J, Harry H, et al. (2010) Brief communication: mitochondrial haplotype C4c confirmed as a founding genome in the Americas. Am J Phys Anthropol 141: 494-497.
35. Perego UA, Lancioni H, Tribaldos M, Angerhofer N, Ekins JE, et al. (2012) Decrypting the mitochondrial gene pool of modern Panamanians. PLoS One 7: e38337.
36. Gómez-Carballa A, Ignacio-Veiga A, Álvarez-Iglesias V, Pastoriza-Mourelle A, Ruiz Y, et al. (2012) A melting pot of multicontinental mtDNA lineages in admixed Venezuelans. Am J Phys Anthropol 147: 78-87.
37. Ginther C, Corach D, Penacino GA, Rey JA, Carnese FR, et al. (1993) Genetic variation among the Mapuche Indians from the Patagonian region of Argentina: mitochondrial DNA sequence variation and allele frequencies of several nuclear genes. EXS 67: 211-219.
38. Horai S, Kondo R, Nakagawa-Hattori Y, Hayashi S, Sonoda S, et al. (1993) Peopling of the Americas, founded by four major lineages of mitochondrial DNA. Mol Biol Evol 10: 23-47.
39. Moraga ML, Rocco P, Miquel JF, Nervi F, Llop E, et al. (2000) Mitochondrial DNA polymorphisms in Chilean aboriginal populations: implications for the peopling of the southern cone of the continent. Am J Phys Anthropol 113: 19-29.
40. Cabana G, Merriwether AD, Hunley K, Demarchi DA, (2006) Is the genetic structure of Gran Chaco populations unique? Interregional perspectives on Native South American mitochondrial DNA variation. Am J Phys Anthropol 131: 108-119.
41. Álvarez-Iglesias V, Jaime JC, Carracedo A, Salas A, (2007) Coding region mitochondrial DNA SNPs: targeting East Asian and Native American haplogroups. Forensic Sci Int Genet 1: 44-55.
42. Bobillo MC, Zimmermann B, Sala A, Huber G, Röck A, et al. (2010) Amerindian mitochondrial DNA haplogroups predominate in the population of Argentina: towards a first nationwide forensic mitochondrial DNA sequence database. Int J Legal Med 124: 263-268.
43. de Saint Pierre M, Bravi CM, Motti JBM, Fuku N, Tanaka M, et al. (2012) An alternative model for the early peopling of southern South America revealed by analyses of three new mitochondrial DNA haplogroups. PLoS One 7: e43486.
44. van Oven M, Kayser M, (2009) Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation. Hum Mutat 30: E386-E394 Available:http://www.phylotree.org.
45. Elson JL, Turnbull DM, Howell N, (2004) Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection. Am J Hum Genet 74: 229-238.
46. Ruiz-Pesini E, Mishmar D, Brandon M, Procaccio V, Wallace DC, (2004) Effects of purifying and adaptive selection on regional variation in human mtDNA. Science 303: 223-226.
47. SMGF (2012) The Sorenson Molecular Genealogy Foundation Mitochondrial Database. Available:http://www.smgf.org. Accessed 2012 Oct 15.
48. EMPOP (2012) European DNA Profiling Group Mitochondrial Population Database. Available:http://www.empop.org. Accessed 2012 Oct 15.
49. Hrdlička A (1925) The Old Americans. Baltimore: Williams & Wilkins Company.
50. Wallace DC, Garrison K, Knowler WC, (1985) Dramatic founder effects in Amerindian mitochondrial DNAs. Am J Phys Anthropol 68: 149-155.
51. Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The history and geography of human genes. Princeton University Press, Princeton, NJ.
52. Pena SD, Santos FR, Bianchi NO, Bravi CM, Carnese FR, et al. (1995) A major founder Y-chromosome haplotype in Amerindians. Nat Genet 11: 15-16.
53. Forster P, Harding R, Torroni A, Bandelt HJ, (1996) Origin and evolution of Native American mtDNA variation: a reappraisal. Am J Hum Genet 59: 935-945.
54. Underhill PA, Jin L, Zemans R, Oefner PJ, Cavalli-Sforza LL, (1996) A pre-Columbian Y chromosome-specific transition and its implications for human evolutionary history. Proc Natl Acad Sci U S A 93: 196-200.
55. Karafet TM, Zegura SL, Posukh O, Osipova L, Bergen A, et al. (1999) Ancestral Asian source(s) of New World Y-chromosome founder haplotypes. Am J Hum Genet 64: 817-831.
56. Santos FR, Pandya A, Tyler-Smith C, Pena SD, Schanfield M, et al. (1999) The Central Siberian origin for native American Y chromosomes. Am J Hum Genet 64: 619-628.
57. Wallace DC, Torroni A, (1992) American Indian prehistory as written in the mitochondrial DNA: a review. Hum Biol 64: 403-416.
58. Achilli A, Rengo C, Magri C, Battaglia V, Olivieri A, et al. (2004) The molecular dissection of mtDNA haplogroup H confirms that the Franco-Cantabrian glacial refuge was a major source for the European gene pool. Am J Hum Genet 75: 910-918.
59. Torroni A, Achilli A, Macaulay V, Richards M, Bandelt HJ, (2006) Harvesting the fruit of the human mtDNA tree. Trends Genet 22: 339-345.
60. Pala M, Achilli A, Olivieri A, Hooshiar Kashani B, Perego UA, et al. (2009) Mitochondrial haplogroup U5b3: a distant echo of the epipaleolithic in Italy and the legacy of the early Sardinians. Am J Hum Genet 84: 814-821.
61. Pala M, Olivieri A, Achilli A, Accetturo M, Metspalu E, et al. (2012) Mitochondrial DNA signals of late glacial recolonization of Europe from near eastern refugia. Am J Hum Genet 90: 915-924.
62. Behar DM, Harmant C, Manry J, van Oven M, Haak W, et al. (2012) The Basque paradigm: genetic evidence of a maternal continuity in the Franco-Cantabrian region since pre-Neolithic times. Am J Hum Genet 90: 486-493.
63. Lalueza C, Pérez-Pérez A, Prats E, Cornudella L, Turbón D, (1997) Lack of founding Amerindian mitochondrial DNA lineages in extinct aborigines from Tierra del Fuego-Patagonia. Hum Mol Genet 6: 41-46.
64. García-Bour J, Pérez-Pérez A, Alvarez S, Fernández E, López-Parra AM, et al. (2004) Early population differentiation in extinct aborigines from Tierra del Fuego-Patagonia: ancient mtDNA sequences and Y-chromosome STR characterization. Am J Phys Anthropol 123: 361-370.
65. Lalueza-Fox C, Calderón FL, Calafell F, Morera B, Bertranpetit J, (2001) MtDNA from extinct Tainos and the peopling of the Caribbean. Ann Hum Genet 65: 137-151.
66. Tarazona-Santos E, Carvalho-Silva DR, Pettener D, Luiselli D, De Stefano GF, et al. (2001) Genetic differentiation in South Amerindians is related to environmental and cultural diversity: Evidence from the Y chromosome. Am J Hum Genet 68: 1485-1496.
67. Wang S, Lewis CM Jr, Jakobsson M, Ramachandran S, Ray N, et al. (2007) Genetic variation and population structure in Native Americans. PLoS Genet 3: e185.
68. Rothhammer F, Dillehay TD, (2009) The late Pleistocene colonization of South America: an interdisciplinary perspective. Ann Hum Genet 73: 540-549.
69. Yang NN, Mazieres S, Bravi C, Ray N, Wang S, et al. (2010) Contrasting patterns of nuclear and mtDNA diversity in Native American populations. Ann Hum Genet 74: 525-538.
70. Reich D, Patterson N, Campbell D, Tandon A, Mazieres S, et al. (2012) Reconstructing Native American population history. Nature 488: 370-374.
71. Luiselli D, Simoni L, Tarazona-Santos E, Pastor S, Pettener D, (2000) Genetic structure of Quechua-speakers of the Central Andes and geographic patterns of gene frequencies in South Amerindian populations. Am J Phys Anthropol 113: 5-17.
72. Rothhammer F, Llop E, Carvallo P, Moraga M, (2001) Origin and evolutionary relationships of native Andean populations. High Alt Med Biol 2: 227-233.
73. Keyeux G, Rodas C, Gelvez N, Carter D, (2002) Possible migration routes into South America deduced from mitochondrial DNA studies in Colombian Amerindian populations. Hum Biol 74: 211-233.
74. Pucciarelli HM, Neves WA, González-José R, Sardi ML, Rozzi FR, et al. (2006) East-West cranial differentiation in pre-Columbian human populations of South America. Homo 57: 133-150.
75. Andrews RM, Kubacka I, Chinnery PF, Lightowlers RN, Turnbull DM, et al. (1999) Reanalysis and revision of the Cambridge reference sequence for human mitochondrial DNA. Nat Genet 23: 147.
76. Torroni A, Rengo C, Guida V, Cruciani F, Sellitto D, et al. (2001) Do the four clades of the mtDNA haplogroup L2 evolve at different rates? Am J Hum Genet 69: 1348-1356.
77. Yang Z, (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.
78. Soares P, Ermini L, Thomson N, Mormina M, Rito T, et al. (2009) Correcting for purifying selection: an improved human mitochondrial molecular clock. Am J Hum Genet 84: 740-759.
79. mtPhyl- software tool for human mtDNA analysis and phylogeny reconstruction. Available:http://eltsov.org. Accessed 2012 Oct 15.
80. Moraga M, de Saint Pierre M, Torres F, Ríos J, (2010) Vínculos de parentesco por vía materna entre los últimos descendientes de la etnia Kawésqar y algunos entierros en los canales patagónicos: evidencia desde el estudio de linajes mitocondriales. Magallania 38: 103-114.
81. Catelli ML, Alvarez-Iglesias V, Gómez-Carballa A, Mosquera-Miguel A, Romanini C, et al. (2011) The impact of modern migrations on present-day multi-ethnic Argentina as recorded on the mitochondrial DNA genome. BMC Genet 12: 77.
82. Salas A, Jaime JC, Alvarez-Iglesias V, Carracedo A, (2008) Gender bias in the multiethnic genetic composition of central Argentina. J Hum Genet 53: 662-674.