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Ancient human genomes suggest three ancestral populations for present-day Europeans

Iosif Lazaridis, Nick Patterson, Alissa Mittnik, Gabriel Renaud, Swapan Mallick, Peter H. Sudmant, Joshua G. Schraiber, Sergi Castellano, Karola Kirsanow, Christos Economou, Ruth Bollongino, Qiaomei Fu, Kirsten I. Bos, Susanne Nordenfelt, Cesare de Filippo, Kay Prüfer, Susanna Sawyer, Cosimo Posth, Wolfgang Haak, Fredrik Hallgren, Elin Fornander, George Ayodo, Hamza A. Babiker, Elena Balanovska, Oleg Balanovsky, Haim Ben-Ami, Judit Bene, Fouad Berrada, Francesca Brisighelli, George Busby, Francesco Cali, Mikhail Churnosov, David E. C. Cole, Larissa Damba, Dominique Delsate, George van Driem, Stanislav Dryomov, Sardana A. Fedorova, Michael Francken, Irene Gallego Romero, Marina Gubina, Jean-Michel Guinet, Michael Hammer, Brenna Henn, Tor Hervig, Ugur Hodoglugil, Aashish R. Jha, Rick Kittles, Elza Khusnutdinova, Toomas Kivisild, Vaidutis Kučinskas, Rita Khusainova, Alena Kushniarevich, Leila Laredj, Sergey Litvinov, Robert W. Mahley, Béla Melegh, Ene Metspalu, Joanna Mountain, Thomas Nyambo, Ludmila Osipova, Jüri Parik, Fedor Platanov, Olga Posukh, Valentino Romano, Igor Rudan, Ruslan Ruizbakiev, Hovhannes Sahakyan, Antonio Salas, Elena B. Starikovskaya, Ayele Tarekegn, Draga Toncheva, Shahlo Turdikulova, Ingrida Uktveryte, Olga Utevska, Mikhail Voevoda, Joachim Wahl, Pierre Zalloua, Levon Yepiskoposyan, Tatijana Zemunik, Alan Cooper, Cristian Capelli, Mark G. Thomas, Sarah A. Tishkoff, Lalji Singh, Kumarasamy Thangaraj, Richard Villems, David Comas, Rem Sukernik, Mait Metspalu, Matthias Meyer, Evan E. Eichler, Joachim Burger, Montgomery Slatkin, Svante Pääbo, Janet Kelso, David Reich, Johannes Krause
doi: https://doi.org/10.1101/001552
Iosif Lazaridis
1Department of Genetics, Harvard Medical School, Boston, MA, USA 02115
2Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142
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Nick Patterson
1Department of Genetics, Harvard Medical School, Boston, MA, USA 02115
2Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142
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Alissa Mittnik
3Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 23, Tübingen, Germany 72072
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Gabriel Renaud
4Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Swapan Mallick
1Department of Genetics, Harvard Medical School, Boston, MA, USA 02115
2Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142
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Peter H. Sudmant
5Department of Genome Sciences, University of Washington, Seattle, WA, USA 98195
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Joshua G. Schraiber
6Department of Integrative Biology, University of California, Berkeley, CA 94720-3140
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Sergi Castellano
4Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Karola Kirsanow
7Johannes Gutenberg University Mainz, Institute of Anthropology, Mainz, Germany D-55128
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Christos Economou
8Archaeological Research Laboratory, Stockholm University, Stockholm, Sweden 114 18
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Ruth Bollongino
7Johannes Gutenberg University Mainz, Institute of Anthropology, Mainz, Germany D-55128
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Qiaomei Fu
4Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Kirsten I. Bos
3Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 23, Tübingen, Germany 72072
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Susanne Nordenfelt
1Department of Genetics, Harvard Medical School, Boston, MA, USA 02115
2Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142
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Cesare de Filippo
4Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Kay Prüfer
4Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Susanna Sawyer
4Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Cosimo Posth
3Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 23, Tübingen, Germany 72072
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Wolfgang Haak
9Australian Centre for Ancient DNA, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia, Australia SA 5005
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Fredrik Hallgren
10The Cultural Heritage Foundation, Västerås, Sweden 722 12
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Elin Fornander
10The Cultural Heritage Foundation, Västerås, Sweden 722 12
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George Ayodo
11Center for Global Health and Child Development, Kisumu, Kenya 40100
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Hamza A. Babiker
12Institutes of Evolution, Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, UK EH9 3JT
13Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alkhod, Muscat, Oman 123
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Elena Balanovska
14Research Centre for Medical Genetics, Moscow, Russia 115478
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Oleg Balanovsky
14Research Centre for Medical Genetics, Moscow, Russia 115478
15Vavilov Institute for General Genetics, Moscow, Russia 119991
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Haim Ben-Ami
16Rambam Health Care Campus, Haifa 31096, Israel
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Judit Bene
17Department of Medical Genetics, and Szentagothai Research Center, University of Pécs, Pécs, Hungary 7624
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Fouad Berrada
18Al Akhawayn University in Ifrane (AUI), School of Science and Engineering, Ifrane, Morocco 53000
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Francesca Brisighelli
19Forensic Genetics Laboratory, Institute of Legal Medicine, Università Cattolica del Sacro Cuore, Rome, Italy 00168
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George Busby
20Department of Zoology, University of Oxford, Oxford, UK OX1 3PS
21Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK OX3 7BN
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Francesco Cali
22Laboratorio di Genetica Molecolare, IRCCS Associazione Oasi Maria SS, Troina Italy 94018
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Mikhail Churnosov
23Belgorod State University, Belgorod, Russia
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David E. C. Cole
24Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada M5G 1L5
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Larissa Damba
25Institute of Internal Medicine, Siberian Branch of Russian Academy of Medical Sciences, Novosibirsk, Russia 630089
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Dominique Delsate
26Luxembourg Natural History Museum, Luxembourg L-2160
27Centre National de Recherche Archéologique auprès du Musée National d’Histoire et d’Art, Luxembourg
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George van Driem
28Institute of Linguistics, University of Bern, Bern, Switzerland CH-3012
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Stanislav Dryomov
29Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, Russian Academy of Science, Siberian Branch, Novosibirsk, Russia 630090
30Institute of Archaeology and Ethnography, Russian Academy of Sciences, Siberian Branch, Novosibirsk, Russia 630090
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Sardana A. Fedorova
31Yakut Research Center of Complex Medical Problems and North-Eastern Federal University, Yakutsk, Russia, 677010
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Michael Francken
32Department of Paleoanthropology, Senckenberg Center for Human Evolution and Paleoenvironment, University of Tübingen, Tübingen, Germany D-72070
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Irene Gallego Romero
33Department of Human Genetics, University of Chicago, Chicago, IL USA 60637
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Marina Gubina
34The Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia 630090
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Jean-Michel Guinet
26Luxembourg Natural History Museum, Luxembourg L-2160
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Michael Hammer
35ARL Division of Biotechnology, University of Arizona, Tucson, AZ, USA 85721
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Brenna Henn
36Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY, USA 11794
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Tor Hervig
37Department of Clinical Science, University of Bergen, Bergen, Norway 5021
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Ugur Hodoglugil
38NextBio, part of Illumina, Santa Clara, CA, USA 95050
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Aashish R. Jha
33Department of Human Genetics, University of Chicago, Chicago, IL USA 60637
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Rick Kittles
39College of Medicine, University of Illinois at Chicago, Chicago, IL, USA 60607
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Elza Khusnutdinova
40Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa, Russia 450054
41Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia 450074
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Toomas Kivisild
42Division of Biological Anthropology, University of Cambridge, Cambridge, United Kingdom CB2 1QH
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Vaidutis Kučinskas
43Department of Human and Medical Genetics, Vilnius University, Vilnius, Lithuania LT-08661
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Rita Khusainova
40Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa, Russia 450054
41Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia 450074
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Alena Kushniarevich
44Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010
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Leila Laredj
45Translational Medicine and Neurogenetics, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France 67404
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Sergey Litvinov
40Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa, Russia 450054
41Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia 450074
44Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010
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Robert W. Mahley
46Robert W. Mahley, Gladstone Institutes, San Francisco, CA 94158
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Béla Melegh
17Department of Medical Genetics, and Szentagothai Research Center, University of Pécs, Pécs, Hungary 7624
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Ene Metspalu
47Department of Evolutionary Biology, University of Tartu, Tartu, Estonia 51010
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Joanna Mountain
48Research Department, 23andMe, Inc. Mountain View, CA, USA 94043
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Thomas Nyambo
49Department of Biochemistry, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania
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Ludmila Osipova
34The Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia 630090
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Jüri Parik
47Department of Evolutionary Biology, University of Tartu, Tartu, Estonia 51010
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Fedor Platanov
50Research Institute of Health, North-Eastern Federal University, Yakutsk, Russia 677000
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Olga Posukh
34The Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia 630090
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Valentino Romano
51Dipartimento di Fisica e Chimica, Università di Palermo, Palermo, Italy 90128
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Igor Rudan
52Centre for Population Health Sciences, The University of Edinburgh Medical School, Edinburgh, Scotland, United Kingdom EH8 9AG
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Ruslan Ruizbakiev
53Deceased: formerly of the Institute of Immunology, Academy of Science, Tashkent, Uzbekistan 70000
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Hovhannes Sahakyan
44Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010
54Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences of Armenia, Yerevan, Armenia 0014
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Antonio Salas
55Unidade de Xenética, Departamento de Anatomía Patolóxica e Ciencias Forenses, and Instituto de Ciencias Forenses, Grupo de Medicina Xenómica (GMX), Facultade de Medicina, Universidade de Santiago de Compostela, Galcia, Spain 15872
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Elena B. Starikovskaya
29Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, Russian Academy of Science, Siberian Branch, Novosibirsk, Russia 630090
30Institute of Archaeology and Ethnography, Russian Academy of Sciences, Siberian Branch, Novosibirsk, Russia 630090
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Ayele Tarekegn
56Addis Ababa University and Center of Human Genetic Diversity, P.O. Box 1176, Addis Ababa, Ethiopia
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Draga Toncheva
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Shahlo Turdikulova
57Institute of Bioorganic Chemistry Academy of Sciences Republic of Uzbekistan, Tashkent, Uzbekistan 100125
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Ingrida Uktveryte
43Department of Human and Medical Genetics, Vilnius University, Vilnius, Lithuania LT-08661
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Olga Utevska
58Department of Genetics and Cytology, V.N. Karazin Kharkiv National University, Kharkiv Ukraine 61077
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Mikhail Voevoda
25Institute of Internal Medicine, Siberian Branch of Russian Academy of Medical Sciences, Novosibirsk, Russia 630089
34The Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia 630090
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Joachim Wahl
59State Office for Cultural Heritage Management Baden-Württemberg, Osteology, Konstanz, Germany D-78467
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Pierre Zalloua
60Lebanese American University, School of Medicine, Beirut, Lebanon 13-5053
61Harvard School of Public Health, Boston, USA 02115
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Levon Yepiskoposyan
54Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences of Armenia, Yerevan, Armenia 0014
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Tatijana Zemunik
62Department of Medical Biology, University of Split, School of Medicine, Split, Croatia 21000
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Alan Cooper
9Australian Centre for Ancient DNA, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia, Australia SA 5005
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Cristian Capelli
21Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK OX3 7BN
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Mark G. Thomas
63Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom WC1E 6BT
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Sarah A. Tishkoff
64Department of Biology and Genetics, University of Pennsylvania, Philadelphia, Pennsylvania, USA 19104
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Lalji Singh
65CSIR-Centre for Cellular and Molecular Biology, Hyderabad, India 500 007
66Present address: Banaras Hindu University, Varanasi, India 221 005
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Kumarasamy Thangaraj
65CSIR-Centre for Cellular and Molecular Biology, Hyderabad, India 500 007
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Richard Villems
44Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010
47Department of Evolutionary Biology, University of Tartu, Tartu, Estonia 51010
67Estonian Academy of Sciences, Tallinn, Estonia 10130
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David Comas
68Institut de Biologia Evolutiva (CSIC-UPF), Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona, Spain 08003
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Rem Sukernik
29Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, Russian Academy of Science, Siberian Branch, Novosibirsk, Russia 630090
30Institute of Archaeology and Ethnography, Russian Academy of Sciences, Siberian Branch, Novosibirsk, Russia 630090
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Mait Metspalu
44Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010
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Matthias Meyer
4Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Evan E. Eichler
5Department of Genome Sciences, University of Washington, Seattle, WA, USA 98195
69Howard Hughes Medical Institute, University of Washington, Seattle, WA, USA 98195
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Joachim Burger
7Johannes Gutenberg University Mainz, Institute of Anthropology, Mainz, Germany D-55128
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Montgomery Slatkin
6Department of Integrative Biology, University of California, Berkeley, CA 94720-3140
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Svante Pääbo
4Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Janet Kelso
4Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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David Reich
1Department of Genetics, Harvard Medical School, Boston, MA, USA 02115
2Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142
70Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA 02115
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Johannes Krause
3Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 23, Tübingen, Germany 72072
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Abstract

Analysis of ancient DNA can reveal historical events that are difficult to discern through study of present-day individuals. To investigate European population history around the time of the agricultural transition, we sequenced complete genomes from a ∼7,500 year old early farmer from the Linearbandkeramik (LBK) culture from Stuttgart in Germany and an ∼8,000 year old hunter-gatherer from the Loschbour rock shelter in Luxembourg. We also generated data from seven ∼8,000 year old hunter-gatherers from Motala in Sweden. We compared these genomes and published ancient DNA to new data from 2,196 samples from 185 diverse populations to show that at least three ancestral groups contributed to present-day Europeans. The first are Ancient North Eurasians (ANE), who are more closely related to Upper Paleolithic Siberians than to any present-day population. The second are West European Hunter-Gatherers (WHG), related to the Loschbour individual, who contributed to all Europeans but not to Near Easterners. The third are Early European Farmers (EEF), related to the Stuttgart individual, who were mainly of Near Eastern origin but also harbored WHG-related ancestry. We model the deep relationships of these populations and show that about ∼44% of the ancestry of EEF derived from a basal Eurasian lineage that split prior to the separation of other non-Africans.

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Posted December 23, 2013.
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Ancient human genomes suggest three ancestral populations for present-day Europeans
Iosif Lazaridis, Nick Patterson, Alissa Mittnik, Gabriel Renaud, Swapan Mallick, Peter H. Sudmant, Joshua G. Schraiber, Sergi Castellano, Karola Kirsanow, Christos Economou, Ruth Bollongino, Qiaomei Fu, Kirsten I. Bos, Susanne Nordenfelt, Cesare de Filippo, Kay Prüfer, Susanna Sawyer, Cosimo Posth, Wolfgang Haak, Fredrik Hallgren, Elin Fornander, George Ayodo, Hamza A. Babiker, Elena Balanovska, Oleg Balanovsky, Haim Ben-Ami, Judit Bene, Fouad Berrada, Francesca Brisighelli, George Busby, Francesco Cali, Mikhail Churnosov, David E. C. Cole, Larissa Damba, Dominique Delsate, George van Driem, Stanislav Dryomov, Sardana A. Fedorova, Michael Francken, Irene Gallego Romero, Marina Gubina, Jean-Michel Guinet, Michael Hammer, Brenna Henn, Tor Hervig, Ugur Hodoglugil, Aashish R. Jha, Rick Kittles, Elza Khusnutdinova, Toomas Kivisild, Vaidutis Kučinskas, Rita Khusainova, Alena Kushniarevich, Leila Laredj, Sergey Litvinov, Robert W. Mahley, Béla Melegh, Ene Metspalu, Joanna Mountain, Thomas Nyambo, Ludmila Osipova, Jüri Parik, Fedor Platanov, Olga Posukh, Valentino Romano, Igor Rudan, Ruslan Ruizbakiev, Hovhannes Sahakyan, Antonio Salas, Elena B. Starikovskaya, Ayele Tarekegn, Draga Toncheva, Shahlo Turdikulova, Ingrida Uktveryte, Olga Utevska, Mikhail Voevoda, Joachim Wahl, Pierre Zalloua, Levon Yepiskoposyan, Tatijana Zemunik, Alan Cooper, Cristian Capelli, Mark G. Thomas, Sarah A. Tishkoff, Lalji Singh, Kumarasamy Thangaraj, Richard Villems, David Comas, Rem Sukernik, Mait Metspalu, Matthias Meyer, Evan E. Eichler, Joachim Burger, Montgomery Slatkin, Svante Pääbo, Janet Kelso, David Reich, Johannes Krause
bioRxiv 001552; doi: https://doi.org/10.1101/001552
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Ancient human genomes suggest three ancestral populations for present-day Europeans
Iosif Lazaridis, Nick Patterson, Alissa Mittnik, Gabriel Renaud, Swapan Mallick, Peter H. Sudmant, Joshua G. Schraiber, Sergi Castellano, Karola Kirsanow, Christos Economou, Ruth Bollongino, Qiaomei Fu, Kirsten I. Bos, Susanne Nordenfelt, Cesare de Filippo, Kay Prüfer, Susanna Sawyer, Cosimo Posth, Wolfgang Haak, Fredrik Hallgren, Elin Fornander, George Ayodo, Hamza A. Babiker, Elena Balanovska, Oleg Balanovsky, Haim Ben-Ami, Judit Bene, Fouad Berrada, Francesca Brisighelli, George Busby, Francesco Cali, Mikhail Churnosov, David E. C. Cole, Larissa Damba, Dominique Delsate, George van Driem, Stanislav Dryomov, Sardana A. Fedorova, Michael Francken, Irene Gallego Romero, Marina Gubina, Jean-Michel Guinet, Michael Hammer, Brenna Henn, Tor Hervig, Ugur Hodoglugil, Aashish R. Jha, Rick Kittles, Elza Khusnutdinova, Toomas Kivisild, Vaidutis Kučinskas, Rita Khusainova, Alena Kushniarevich, Leila Laredj, Sergey Litvinov, Robert W. Mahley, Béla Melegh, Ene Metspalu, Joanna Mountain, Thomas Nyambo, Ludmila Osipova, Jüri Parik, Fedor Platanov, Olga Posukh, Valentino Romano, Igor Rudan, Ruslan Ruizbakiev, Hovhannes Sahakyan, Antonio Salas, Elena B. Starikovskaya, Ayele Tarekegn, Draga Toncheva, Shahlo Turdikulova, Ingrida Uktveryte, Olga Utevska, Mikhail Voevoda, Joachim Wahl, Pierre Zalloua, Levon Yepiskoposyan, Tatijana Zemunik, Alan Cooper, Cristian Capelli, Mark G. Thomas, Sarah A. Tishkoff, Lalji Singh, Kumarasamy Thangaraj, Richard Villems, David Comas, Rem Sukernik, Mait Metspalu, Matthias Meyer, Evan E. Eichler, Joachim Burger, Montgomery Slatkin, Svante Pääbo, Janet Kelso, David Reich, Johannes Krause
bioRxiv 001552; doi: https://doi.org/10.1101/001552

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