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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
Department of Genetics, Harvard Medical School, Boston, MA, USA 02115Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142
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Nick Patterson
Department of Genetics, Harvard Medical School, Boston, MA, USA 02115Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142
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Alissa Mittnik
Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 23, Tübingen, Germany 72072
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Gabriel Renaud
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Swapan Mallick
Department of Genetics, Harvard Medical School, Boston, MA, USA 02115Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142
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Peter H. Sudmant
Department of Genome Sciences, University of Washington, Seattle, WA, USA 98195
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Joshua G. Schraiber
Department of Integrative Biology, University of California, Berkeley, CA 94720-3140
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Sergi Castellano
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Karola Kirsanow
Johannes Gutenberg University Mainz, Institute of Anthropology, Mainz, Germany D-55128
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Christos Economou
Archaeological Research Laboratory, Stockholm University, Stockholm, Sweden 114 18
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Ruth Bollongino
Johannes Gutenberg University Mainz, Institute of Anthropology, Mainz, Germany D-55128
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Qiaomei Fu
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Kirsten I. Bos
Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 23, Tübingen, Germany 72072
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Susanne Nordenfelt
Department of Genetics, Harvard Medical School, Boston, MA, USA 02115Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142
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Cesare de Filippo
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Kay Prüfer
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Susanna Sawyer
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Cosimo Posth
Institute for Archaeological Sciences, University of Tübingen, Rümelinstrasse 23, Tübingen, Germany 72072
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Wolfgang Haak
Australian 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
The Cultural Heritage Foundation, Västerås, Sweden 722 12
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Elin Fornander
The Cultural Heritage Foundation, Västerås, Sweden 722 12
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George Ayodo
Center for Global Health and Child Development, Kisumu, Kenya 40100
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Hamza A. Babiker
Institutes of Evolution, Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh, UK EH9 3JTBiochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alkhod, Muscat, Oman 123
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Elena Balanovska
Research Centre for Medical Genetics, Moscow, Russia 115478
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Oleg Balanovsky
Research Centre for Medical Genetics, Moscow, Russia 115478Vavilov Institute for General Genetics, Moscow, Russia 119991
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Haim Ben-Ami
Rambam Health Care Campus, Haifa 31096, Israel
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Judit Bene
Department of Medical Genetics, and Szentagothai Research Center, University of Pécs, Pécs, Hungary 7624
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Fouad Berrada
Al Akhawayn University in Ifrane (AUI), School of Science and Engineering, Ifrane, Morocco 53000
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Francesca Brisighelli
Forensic Genetics Laboratory, Institute of Legal Medicine, Università Cattolica del Sacro Cuore, Rome, Italy 00168
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George Busby
Department of Zoology, University of Oxford, Oxford, UK OX1 3PSWellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK OX3 7BN
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Francesco Cali
Laboratorio di Genetica Molecolare, IRCCS Associazione Oasi Maria SS, Troina Italy 94018
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Mikhail Churnosov
Belgorod State University, Belgorod, Russia
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David E. C. Cole
Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario, Canada M5G 1L5
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Larissa Damba
Institute of Internal Medicine, Siberian Branch of Russian Academy of Medical Sciences, Novosibirsk, Russia 630089
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Dominique Delsate
Luxembourg Natural History Museum, Luxembourg L-2160Centre National de Recherche Archéologique auprès du Musée National d’Histoire et d’Art, Luxembourg
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George van Driem
Institute of Linguistics, University of Bern, Bern, Switzerland CH-3012
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Stanislav Dryomov
Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, Russian Academy of Science, Siberian Branch, Novosibirsk, Russia 630090Institute of Archaeology and Ethnography, Russian Academy of Sciences, Siberian Branch, Novosibirsk, Russia 630090
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Sardana A. Fedorova
Yakut Research Center of Complex Medical Problems and North-Eastern Federal University, Yakutsk, Russia, 677010
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Michael Francken
Department of Paleoanthropology, Senckenberg Center for Human Evolution and Paleoenvironment, University of Tübingen, Tübingen, Germany D-72070
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Irene Gallego Romero
Department of Human Genetics, University of Chicago, Chicago, IL USA 60637
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Marina Gubina
The Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia 630090
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Jean-Michel Guinet
Luxembourg Natural History Museum, Luxembourg L-2160
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Michael Hammer
ARL Division of Biotechnology, University of Arizona, Tucson, AZ, USA 85721
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Brenna Henn
Department of Ecology and Evolution, Stony Brook University, Stony Brook, NY, USA 11794
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Tor Hervig
Department of Clinical Science, University of Bergen, Bergen, Norway 5021
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Ugur Hodoglugil
NextBio, part of Illumina, Santa Clara, CA, USA 95050
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Aashish R. Jha
Department of Human Genetics, University of Chicago, Chicago, IL USA 60637
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Rick Kittles
College of Medicine, University of Illinois at Chicago, Chicago, IL, USA 60607
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Elza Khusnutdinova
Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa, Russia 450054Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia 450074
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Toomas Kivisild
Division of Biological Anthropology, University of Cambridge, Cambridge, United Kingdom CB2 1QH
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Vaidutis Kučinskas
Department of Human and Medical Genetics, Vilnius University, Vilnius, Lithuania LT-08661
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Rita Khusainova
Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa, Russia 450054Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia 450074
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Alena Kushniarevich
Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010
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Leila Laredj
Translational Medicine and Neurogenetics, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch, France 67404
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Sergey Litvinov
Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa, Russia 450054Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa, Russia 450074Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010
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Robert W. Mahley
Robert W. Mahley, Gladstone Institutes, San Francisco, CA 94158
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Béla Melegh
Department of Medical Genetics, and Szentagothai Research Center, University of Pécs, Pécs, Hungary 7624
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Ene Metspalu
Department of Evolutionary Biology, University of Tartu, Tartu, Estonia 51010
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Joanna Mountain
Research Department, 23andMe, Inc. Mountain View, CA, USA 94043
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Thomas Nyambo
Department of Biochemistry, Muhimbili University of Health and Allied Sciences, Dar es Salaam, Tanzania
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Ludmila Osipova
The Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia 630090
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Jüri Parik
Department of Evolutionary Biology, University of Tartu, Tartu, Estonia 51010
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Fedor Platanov
Research Institute of Health, North-Eastern Federal University, Yakutsk, Russia 677000
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Olga Posukh
The Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia 630090
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Valentino Romano
Dipartimento di Fisica e Chimica, Università di Palermo, Palermo, Italy 90128
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Igor Rudan
Centre for Population Health Sciences, The University of Edinburgh Medical School, Edinburgh, Scotland, United Kingdom EH8 9AG
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Ruslan Ruizbakiev
Deceased: formerly of the Institute of Immunology, Academy of Science, Tashkent, Uzbekistan 70000
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Hovhannes Sahakyan
Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences of Armenia, Yerevan, Armenia 0014
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Antonio Salas
Unidade 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
Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, Russian Academy of Science, Siberian Branch, Novosibirsk, Russia 630090Institute of Archaeology and Ethnography, Russian Academy of Sciences, Siberian Branch, Novosibirsk, Russia 630090
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Ayele Tarekegn
Addis 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
Institute of Bioorganic Chemistry Academy of Sciences Republic of Uzbekistan, Tashkent, Uzbekistan 100125
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Ingrida Uktveryte
Department of Human and Medical Genetics, Vilnius University, Vilnius, Lithuania LT-08661
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Olga Utevska
Department of Genetics and Cytology, V.N. Karazin Kharkiv National University, Kharkiv Ukraine 61077
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Mikhail Voevoda
Institute of Internal Medicine, Siberian Branch of Russian Academy of Medical Sciences, Novosibirsk, Russia 630089The Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia 630090
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Joachim Wahl
State Office for Cultural Heritage Management Baden-Württemberg, Osteology, Konstanz, Germany D-78467
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Pierre Zalloua
Lebanese American University, School of Medicine, Beirut, Lebanon 13-5053Harvard School of Public Health, Boston, USA 02115
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Levon Yepiskoposyan
Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences of Armenia, Yerevan, Armenia 0014
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Tatijana Zemunik
Department of Medical Biology, University of Split, School of Medicine, Split, Croatia 21000
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Alan Cooper
Australian 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
Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford, UK OX3 7BN
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Mark G. Thomas
Research Department of Genetics, Evolution and Environment, University College London, London, United Kingdom WC1E 6BT
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Sarah A. Tishkoff
Department of Biology and Genetics, University of Pennsylvania, Philadelphia, Pennsylvania, USA 19104
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Lalji Singh
CSIR-Centre for Cellular and Molecular Biology, Hyderabad, India 500 007Present address: Banaras Hindu University, Varanasi, India 221 005
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Kumarasamy Thangaraj
CSIR-Centre for Cellular and Molecular Biology, Hyderabad, India 500 007
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Richard Villems
Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010Department of Evolutionary Biology, University of Tartu, Tartu, Estonia 51010Estonian Academy of Sciences, Tallinn, Estonia 10130
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David Comas
Institut 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
Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, Russian Academy of Science, Siberian Branch, Novosibirsk, Russia 630090Institute of Archaeology and Ethnography, Russian Academy of Sciences, Siberian Branch, Novosibirsk, Russia 630090
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Mait Metspalu
Estonian Biocentre, Evolutionary Biology group, Tartu, Estonia 51010
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Matthias Meyer
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Evan E. Eichler
Department of Genome Sciences, University of Washington, Seattle, WA, USA 98195Howard Hughes Medical Institute, University of Washington, Seattle, WA, USA 98195
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Joachim Burger
Johannes Gutenberg University Mainz, Institute of Anthropology, Mainz, Germany D-55128
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Montgomery Slatkin
Department of Integrative Biology, University of California, Berkeley, CA 94720-3140
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Svante Pääbo
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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Janet Kelso
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 04103
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David Reich
Department of Genetics, Harvard Medical School, Boston, MA, USA 02115Broad Institute of Harvard and MIT, Cambridge, MA, USA 02142Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA 02115
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Johannes Krause
Institute 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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