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Research Article

Reconciling migration models to the Americas with the variation of North American native mitogenomes

Alessandro Achilli, Ugo A. Perego, Hovirag Lancioni, Anna Olivieri, Francesca Gandini, Baharak Hooshiar Kashani, Vincenza Battaglia, Viola Grugni, Norman Angerhofer, Mary P. Rogers, Rene J. Herrera, Scott R. Woodward, Damian Labuda, David Glenn Smith, Jerome S. Cybulski, Ornella Semino, Ripan S. Malhi, and Antonio Torroni
PNAS first published August 12, 2013; https://doi.org/10.1073/pnas.1306290110
Alessandro Achilli
aDipartimento di Chimica, Biologia e Biotecnologie, Università di Perugia, 06123 Perugia, Italy;
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  • For correspondence: alessandro.achilli@unipg.it antonio.torroni@unipv.it
Ugo A. Perego
bDipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, Università di Pavia, 27100 Pavia, Italy;
cSorenson Molecular Genealogy Foundation, Salt Lake City, UT 84115;
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Hovirag Lancioni
aDipartimento di Chimica, Biologia e Biotecnologie, Università di Perugia, 06123 Perugia, Italy;
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Anna Olivieri
bDipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, Università di Pavia, 27100 Pavia, Italy;
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Francesca Gandini
bDipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, Università di Pavia, 27100 Pavia, Italy;
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Baharak Hooshiar Kashani
bDipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, Università di Pavia, 27100 Pavia, Italy;
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Vincenza Battaglia
bDipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, Università di Pavia, 27100 Pavia, Italy;
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Viola Grugni
bDipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, Università di Pavia, 27100 Pavia, Italy;
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Norman Angerhofer
cSorenson Molecular Genealogy Foundation, Salt Lake City, UT 84115;
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Mary P. Rogers
dDepartment of Anthropology and
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Rene J. Herrera
eDepartment of Biological Sciences, Florida International University, Miami, FL 33199;
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Scott R. Woodward
cSorenson Molecular Genealogy Foundation, Salt Lake City, UT 84115;
fAncestryDNA, Provo, UT 84604;
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Damian Labuda
gDépartement de Pédiatrie, Centre de Recherche du Centre Hospitalier Universitaire Sainte-Justine, Université de Montréal, Montréal, QC, Canada H3T 1C5;
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David Glenn Smith
hDepartment of Anthropology, University of California, Davis, CA 95616; and
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Jerome S. Cybulski
iCanadian Museum of Civilization, Gatineau, QC, Canada K1A 0M8
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Ornella Semino
bDipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, Università di Pavia, 27100 Pavia, Italy;
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Ripan S. Malhi
dDepartment of Anthropology and
jInstitute for Genomic Biology, University of Illinois, Champaign, IL 61801;
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Antonio Torroni
bDipartimento di Biologia e Biotecnologie “Lazzaro Spallanzani”, Università di Pavia, 27100 Pavia, Italy;
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  • For correspondence: alessandro.achilli@unipg.it antonio.torroni@unipv.it
  1. Edited by Francisco Mauro Salzano, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil, and approved July 16, 2013 (received for review April 8, 2013)

This article has a Letter. Please see:

  • Reconciling pre-Columbian settlement hypotheses requires integrative, multidisciplinary, and model-bound approaches - January 07, 2014
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Abstract

In this study we evaluated migration models to the Americas by using the information contained in native mitochondrial genomes (mitogenomes) from North America. Molecular and phylogeographic analyses of B2a mitogenomes, which are absent in Eskimo–Aleut and northern Na-Dene speakers, revealed that this haplogroup arose in North America ∼11–13 ka from one of the founder Paleo-Indian B2 mitogenomes. In contrast, haplogroup A2a, which is typical of Eskimo–Aleuts and Na-Dene, but also present in the easternmost Siberian groups, originated only 4–7 ka in Alaska, led to the first Paleo-Eskimo settlement of northern Canada and Greenland, and contributed to the formation of the Na-Dene gene pool. However, mitogenomes also show that Amerindians from northern North America, without any distinction between Na-Dene and non–Na-Dene, were heavily affected by an additional and distinctive Beringian genetic input. In conclusion, most mtDNA variation (along the double-continent) stems from the first wave from Beringia, which followed the Pacific coastal route. This was accompanied or followed by a second inland migratory event, marked by haplogroups X2a and C4c, which affected all Amerindian groups of Northern North America. Much later, the ancestral A2a carriers spread from Alaska, undertaking both a westward migration to Asia and an eastward expansion into the circumpolar regions of Canada. Thus, the first American founders left the greatest genetic mark but the original maternal makeup of North American Natives was subsequently reshaped by additional streams of gene flow and local population dynamics, making a three-wave view too simplistic.

  • Native Americans
  • human mtDNA

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: alessandro.achilli{at}unipg.it or antonio.torroni{at}unipv.it.
  • Author contributions: A.A., U.A.P., R.S.M., and A.T. designed research; A.A., U.A.P., H.L., A.O., F.G., B.H.K., V.B., V.G., and M.P.R. performed research; A.A., R.J.H., S.R.W., D.L., D.G.S., J.S.C., O.S., R.S.M., and A.T. contributed new reagents/analytic tools; A.A., U.A.P., H.L., A.O., N.A., and A.T. analyzed data; and A.A., U.A.P., D.L., O.S., R.S.M., and A.T. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KC710999–KC711039).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1306290110/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Origin of North American native mitogenomes
Alessandro Achilli, Ugo A. Perego, Hovirag Lancioni, Anna Olivieri, Francesca Gandini, Baharak Hooshiar Kashani, Vincenza Battaglia, Viola Grugni, Norman Angerhofer, Mary P. Rogers, Rene J. Herrera, Scott R. Woodward, Damian Labuda, David Glenn Smith, Jerome S. Cybulski, Ornella Semino, Ripan S. Malhi, Antonio Torroni
Proceedings of the National Academy of Sciences Aug 2013, 201306290; DOI: 10.1073/pnas.1306290110

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Origin of North American native mitogenomes
Alessandro Achilli, Ugo A. Perego, Hovirag Lancioni, Anna Olivieri, Francesca Gandini, Baharak Hooshiar Kashani, Vincenza Battaglia, Viola Grugni, Norman Angerhofer, Mary P. Rogers, Rene J. Herrera, Scott R. Woodward, Damian Labuda, David Glenn Smith, Jerome S. Cybulski, Ornella Semino, Ripan S. Malhi, Antonio Torroni
Proceedings of the National Academy of Sciences Aug 2013, 201306290; DOI: 10.1073/pnas.1306290110
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