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Research Article

Maternal traces of deep common ancestry and asymmetric gene flow between Pygmy hunter–gatherers and Bantu-speaking farmers

Lluís Quintana-Murci, Hélène Quach, Christine Harmant, Francesca Luca, Blandine Massonnet, Etienne Patin, Lucas Sica, Patrick Mouguiama-Daouda, David Comas, Shay Tzur, Oleg Balanovsky, Kenneth K. Kidd, Judith R. Kidd, Lolke van der Veen, Jean-Marie Hombert, Antoine Gessain, Paul Verdu, Alain Froment, Serge Bahuchet, Evelyne Heyer, Jean Dausset, Antonio Salas, and Doron M. Behar
  1. aHuman Evolutionary Genetics Unit, Centre National de la Recherche Scientifique URA3012, Institut Pasteur, 75015 Paris, France;
  2. cCentre International de Recherches Médicales de Franceville, BP769 Franceville, Gabon;
  3. dUnité Mixte de Recherche 5596, Institut des Sciences de l'Homme, 69363 Lyon, France;
  4. eUnitat de Biologia Evolutiva, Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, 08003 Barcelona, Spain;
  5. fMolecular Medicine Laboratory, Rambam Health Care Campus, Haifa 31096, Israel;
  6. gRussian Academy of Medical Sciences, 109544 Moscow, Russia;
  7. hDepartment of Genetics, Yale University School of Medicine, SHM I-353, New Haven, CT 06510;
  8. iUnité d'Epidémiologie et Physiopathologie des Virus Oncogènes, Institut Pasteur, 75015 Paris, France;
  9. jMuséum National d'Histoire Naturelle–Centre National de la Recherche Scientifique-P7 Unité Mixte de Recherche 5145, Eco-Anthropologie, Musée de l'Homme, 75016 Paris, France;
  10. kFondation Jean Dausset, Centre d'Etude du Polymorphisme Humain, 75010 Paris, France; and
  11. lUnidade de Xenética, Instituto de Medicina Legal, Universidad de Santiago de Compostela, 15782 Galicia, Spain

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PNAS February 5, 2008 105 (5) 1596-1601; https://doi.org/10.1073/pnas.0711467105
Lluís Quintana-Murci
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  • For correspondence: quintana@pasteur.fr dausset@cephb.fr
Hélène Quach
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Christine Harmant
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Francesca Luca
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Blandine Massonnet
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Etienne Patin
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Lucas Sica
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Patrick Mouguiama-Daouda
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David Comas
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Shay Tzur
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Oleg Balanovsky
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Kenneth K. Kidd
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Judith R. Kidd
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Lolke van der Veen
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Jean-Marie Hombert
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Antoine Gessain
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Paul Verdu
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Alain Froment
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Serge Bahuchet
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Evelyne Heyer
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Jean Dausset
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  • For correspondence: quintana@pasteur.fr dausset@cephb.fr
Antonio Salas
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Doron M. Behar
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  1. Contributed by Jean Dausset, December 6, 2007 (received for review October 12, 2007)

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Abstract

Two groups of populations with completely different lifestyles—the Pygmy hunter–gatherers and the Bantu-speaking farmers—coexist in Central Africa. We investigated the origins of these two groups and the interactions between them, by analyzing mtDNA variation in 1,404 individuals from 20 farming populations and 9 Pygmy populations from Central Africa, with the aim of shedding light on one of the most fascinating cultural transitions in human evolution (the transition from hunting and gathering to agriculture). Our data indicate that this region was colonized gradually, with an initial L1c-rich ancestral population ultimately giving rise to current-day farmers, who display various L1c clades, and to Pygmies, in whom L1c1a is the only surviving clade. Detailed phylogenetic analysis of complete mtDNA sequences for L1c1a showed this clade to be autochthonous to Central Africa, with its most recent branches shared between farmers and Pygmies. Coalescence analyses revealed that these two groups arose through a complex evolutionary process characterized by (i) initial divergence of the ancestors of contemporary Pygmies from an ancestral Central African population no more than ≈70,000 years ago, (ii) a period of isolation between the two groups, accounting for their phenotypic differences, (iii) long-standing asymmetric maternal gene flow from Pygmies to the ancestors of the farming populations, beginning no more than ≈40,000 years ago and persisting until a few thousand years ago, and (iv) enrichment of the maternal gene pool of the ancestors of the farming populations by the arrival and/or subsequent demographic expansion of L0a, L2, and L3 carriers.

  • Africa
  • evolution
  • human
  • mtDNA
  • populations

Footnotes

  • bTo whom correspondence may be addressed. E-mail: quintana{at}pasteur.fr or dausset{at}cephb.fr
  • Author contributions: L.Q.-M. designed research; H.Q., C.H., F.L., and B.M. performed research; E.P., L.S., P.M.-D., D.C., S.T., O.B., K.K.K., J.R.K., L.v.d.V., J.-M.H., A.G., P.V., A.F., S.B., E.H., and J.D. contributed new reagents/analytic tools; L.Q.-M. and D.M.B. analyzed data; and L.Q.-M., A.S., and D.M.B. wrote the paper.

  • The authors declare no conflict of interest.

  • Data deposition: The complete mtDNA sequences reported in this paper have been deposited in the GenBank database (accession nos. EU273476–EU273502).

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0711467105/DC1.

  • Freely available online through the PNAS open access option.

  • © 2008 by The National Academy of Sciences of the USA
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Maternal traces of deep common ancestry and asymmetric gene flow between Pygmy hunter–gatherers and Bantu-speaking farmers
Lluís Quintana-Murci, Hélène Quach, Christine Harmant, Francesca Luca, Blandine Massonnet, Etienne Patin, Lucas Sica, Patrick Mouguiama-Daouda, David Comas, Shay Tzur, Oleg Balanovsky, Kenneth K. Kidd, Judith R. Kidd, Lolke van der Veen, Jean-Marie Hombert, Antoine Gessain, Paul Verdu, Alain Froment, Serge Bahuchet, Evelyne Heyer, Jean Dausset, Antonio Salas, Doron M. Behar
Proceedings of the National Academy of Sciences Feb 2008, 105 (5) 1596-1601; DOI: 10.1073/pnas.0711467105

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Maternal traces of deep common ancestry and asymmetric gene flow between Pygmy hunter–gatherers and Bantu-speaking farmers
Lluís Quintana-Murci, Hélène Quach, Christine Harmant, Francesca Luca, Blandine Massonnet, Etienne Patin, Lucas Sica, Patrick Mouguiama-Daouda, David Comas, Shay Tzur, Oleg Balanovsky, Kenneth K. Kidd, Judith R. Kidd, Lolke van der Veen, Jean-Marie Hombert, Antoine Gessain, Paul Verdu, Alain Froment, Serge Bahuchet, Evelyne Heyer, Jean Dausset, Antonio Salas, Doron M. Behar
Proceedings of the National Academy of Sciences Feb 2008, 105 (5) 1596-1601; DOI: 10.1073/pnas.0711467105
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