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

doi:10.1038/nature13673

. 2014 Sep 18;513(7518):409-13.

doi: 10.1038/nature13673.

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

Iosif Lazaridis¹, Nick Patterson², Alissa Mittnik³, Gabriel Renaud⁴, Swapan Mallick¹, Karola Kirsanow⁵, Peter H Sudmant⁶, Joshua G Schraiber⁷, Sergi Castellano⁴, Mark Lipson⁸, Bonnie Berger⁹, Christos Economou¹⁰, Ruth Bollongino⁵, Qiaomei Fu¹¹, Kirsten I Bos³, Susanne Nordenfelt¹, Heng Li¹, Cesare de Filippo⁴, Kay Prüfer⁴, Susanna Sawyer⁴, Cosimo Posth³, Wolfgang Haak¹², Fredrik Hallgren¹³, Elin Fornander¹³, Nadin Rohland¹, Dominique Delsate¹⁴, Michael Francken¹⁵, Jean-Michel Guinet¹⁶, Joachim Wahl¹⁷, George Ayodo¹⁸, Hamza A Babiker¹⁹, Graciela Bailliet²⁰, Elena Balanovska²¹, Oleg Balanovsky²², Ramiro Barrantes²³, Gabriel Bedoya²⁴, Haim Ben-Ami²⁵, Judit Bene²⁶, Fouad Berrada²⁷, Claudio M Bravi²⁰, Francesca Brisighelli²⁸, George B J Busby²⁹, Francesco Cali³⁰, Mikhail Churnosov³¹, David E C Cole³², Daniel Corach³³, Larissa Damba³⁴, George van Driem³⁵, Stanislav Dryomov³⁶, Jean-Michel Dugoujon³⁷, Sardana A Fedorova³⁸, Irene Gallego Romero³⁹, Marina Gubina³⁴, Michael Hammer⁴⁰, Brenna M Henn⁴¹, Tor Hervig⁴², Ugur Hodoglugil⁴³, Aashish R Jha³⁹, Sena Karachanak-Yankova⁴⁴, Rita Khusainova⁴⁵, Elza Khusnutdinova⁴⁵, Rick Kittles⁴⁶, Toomas Kivisild⁴⁷, William Klitz⁴⁸, Vaidutis Kučinskas⁴⁹, Alena Kushniarevich⁵⁰, Leila Laredj⁵¹, Sergey Litvinov⁵², Theologos Loukidis⁵³, Robert W Mahley⁵⁴, Béla Melegh²⁶, Ene Metspalu⁵⁵, Julio Molina⁵⁶, Joanna Mountain⁵⁷, Klemetti Näkkäläjärvi⁵⁸, Desislava Nesheva⁴⁴, Thomas Nyambo⁵⁹, Ludmila Osipova³⁴, Jüri Parik⁵⁵, Fedor Platonov⁶⁰, Olga Posukh³⁴, Valentino Romano⁶¹, Francisco Rothhammer⁶², Igor Rudan⁶³, Ruslan Ruizbakiev⁶⁴, Hovhannes Sahakyan⁶⁵, Antti Sajantila⁶⁶, Antonio Salas⁶⁷, Elena B Starikovskaya³⁶, Ayele Tarekegn⁶⁸, Draga Toncheva⁴⁴, Shahlo Turdikulova⁶⁹, Ingrida Uktveryte⁴⁹, Olga Utevska⁷⁰, René Vasquez⁷¹, Mercedes Villena⁷¹, Mikhail Voevoda⁷², Cheryl A Winkler⁷³, Levon Yepiskoposyan⁷⁴, Pierre Zalloua⁷⁵, Tatijana Zemunik⁷⁶, Alan Cooper¹², Cristian Capelli⁷⁷, Mark G Thomas⁷⁸, Andres Ruiz-Linares⁷⁸, Sarah A Tishkoff⁷⁹, Lalji Singh⁸⁰, Kumarasamy Thangaraj⁸¹, Richard Villems⁸², David Comas⁸³, Rem Sukernik³⁶, Mait Metspalu⁵⁰, Matthias Meyer⁴, Evan E Eichler⁸⁴, Joachim Burger⁵, Montgomery Slatkin⁴⁸, Svante Pääbo⁴, Janet Kelso⁴, David Reich⁸⁵, Johannes Krause⁸⁶

Affiliations

¹ 1] Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA. [2] Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA.
² Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA.
³ Institute for Archaeological Sciences, University of Tübingen, Tübingen 72074, Germany.
⁴ Max Planck Institute for Evolutionary Anthropology, Leipzig 04103, Germany.
⁵ Institute of Anthropology, Johannes Gutenberg University Mainz, Mainz D-55128, Germany.
⁶ Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA.
⁷ 1] Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA. [2] Department of Integrative Biology, University of California, Berkeley, California 94720-3140, USA.
⁸ Department of Mathematics and Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
⁹ 1] Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA. [2] Department of Mathematics and Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
¹⁰ Archaeological Research Laboratory, Stockholm University, 114 18, Sweden.
¹¹ 1] Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA. [2] Max Planck Institute for Evolutionary Anthropology, Leipzig 04103, Germany. [3] Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, IVPP, CAS, Beijing 100049, China.
¹² Australian Centre for Ancient DNA and Environment Institute, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia.
¹³ The Cultural Heritage Foundation, Västerås 722 12, Sweden.
¹⁴ 1] National Museum of Natural History, L-2160, Luxembourg. [2] National Center of Archaeological Research, National Museum of History and Art, L-2345, Luxembourg.
¹⁵ Department of Paleoanthropology, Senckenberg Center for Human Evolution and Paleoenvironment, University of Tübingen, Tübingen D-72070, Germany.
¹⁶ National Museum of Natural History, L-2160, Luxembourg.
¹⁷ State Office for Cultural Heritage Management Baden-Württemberg, Osteology, Konstanz D-78467, Germany.
¹⁸ Center for Global Health and Child Development, Kisumu 40100, Kenya.
¹⁹ 1] Institutes of Evolution, Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JT, UK. [2] Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alkhod, Muscat 123, Oman.
²⁰ Laboratorio de Genética Molecular Poblacional, Instituto Multidisciplinario de Biología Celular (IMBICE), CCT-CONICET &CICPBA, La Plata, B1906APO, Argentina.
²¹ Research Centre for Medical Genetics, Moscow 115478, Russia.
²² 1] Research Centre for Medical Genetics, Moscow 115478, Russia. [2] Vavilov Institute for General Genetics, Moscow 119991, Russia.
²³ Escuela de Biología, Universidad de Costa Rica, San José 2060, Costa Rica.
²⁴ Institute of Biology, Research group GENMOL, Universidad de Antioquia, Medellín, Colombia.
²⁵ Rambam Health Care Campus, Haifa 31096, Israel.
²⁶ Department of Medical Genetics and Szentagothai Research Center, University of Pécs, Pécs H-7624, Hungary.
²⁷ Al Akhawayn University in Ifrane (AUI), School of Science and Engineering, Ifrane 53000, Morocco.
²⁸ Forensic Genetics Laboratory, Institute of Legal Medicine, Università Cattolica del Sacro Cuore, Rome 00168, Italy.
²⁹ 1] Department of Zoology, University of Oxford, Oxford OX1 3PS, UK. [2] Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, UK.
³⁰ Laboratorio di Genetica Molecolare, IRCCS Associazione Oasi Maria SS, Troina 94018, Italy.
³¹ Belgorod State University, Belgorod 308015, Russia.
³² Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario M5G 1L5, Canada.
³³ Servicio de Huellas Digitales Genéticas, School of Pharmacy and Biochemistry, Universidad de Buenos Aires, 1113 CABA, Argentina.
³⁴ Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia.
³⁵ Institute of Linguistics, University of Bern, Bern CH-3012, Switzerland.
³⁶ Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, Russian Academy of Science, Siberian Branch, Novosibirsk 630090, Russia.
³⁷ Anthropologie Moléculaire et Imagerie de Synthèse, CNRS UMR 5288, Université Paul Sabatier Toulouse III, Toulouse 31000, France.
³⁸ North-Eastern Federal University and Yakut Research Center of Complex Medical Problems, Yakutsk 677013, Russia.
³⁹ Department of Human Genetics, University of Chicago, Chicago, Illinois 60637, USA.
⁴⁰ ARL Division of Biotechnology, University of Arizona, Tucson, Arizona 85721, USA.
⁴¹ Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York 11794, USA.
⁴² Department of Clinical Science, University of Bergen, Bergen 5021, Norway.
⁴³ NextBio, Illumina, Santa Clara, California 95050, USA.
⁴⁴ Department of Medical Genetics, National Human Genome Center, Medical University Sofia, Sofia 1431, Bulgaria.
⁴⁵ 1] Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa 450054, Russia. [2] Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa 450074, Russia.
⁴⁶ College of Medicine, University of Arizona, Tucson, Arizona 85724, USA.
⁴⁷ Division of Biological Anthropology, University of Cambridge, Cambridge CB2 1QH, UK.
⁴⁸ Department of Integrative Biology, University of California, Berkeley, California 94720-3140, USA.
⁴⁹ Department of Human and Medical Genetics, Vilnius University, Vilnius LT-08661, Lithuania.
⁵⁰ Estonian Biocentre, Evolutionary Biology group, Tartu, 51010, Estonia.
⁵¹ Translational Medicine and Neurogenetics, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch 67404, France.
⁵² 1] Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa 450054, Russia. [2] Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa 450074, Russia. [3] Estonian Biocentre, Evolutionary Biology group, Tartu, 51010, Estonia.
⁵³ 1] Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK. [2] Amgen, 33 Kazantzaki Str, Ilioupolis 16342, Athens, Greece (T.L.); Banaras Hindu University, Varanasi 221 005, India (L.S.).
⁵⁴ Gladstone Institutes, San Francisco, California 94158, USA.
⁵⁵ Department of Evolutionary Biology, University of Tartu, Tartu 51010, Estonia.
⁵⁶ Centro de Investigaciones Biomédicas de Guatemala, Ciudad de Guatemala, Guatemala.
⁵⁷ Research Department, 23andMe, Mountain View, California 94043, USA.
⁵⁸ Cultural Anthropology Program, University of Oulu, Oulu 90014, Finland.
⁵⁹ Department of Biochemistry, Muhimbili University of Health and Allied Sciences, Dar es Salaam 65001, Tanzania.
⁶⁰ Research Institute of Health, North-Eastern Federal University, Yakutsk 677000, Russia.
⁶¹ Dipartimento di Fisica e Chimica, Università di Palermo, Palermo 90128, Italy.
⁶² 1] Instituto de Alta Investigación, Universidad de Tarapacá, Arica 1000000, Chile. [2] Programa de Genética Humana ICBM Facultad de Medicina Universidad de Chile, Santiago 8320000, Chile. [3] Centro de Investigaciones del Hombre en el Desierto, Arica 1000000, Chile.
⁶³ Centre for Population Health Sciences, The University of Edinburgh Medical School, Edinburgh EH8 9AG, UK.
⁶⁴ 1] Institute of Immunology, Academy of Science, Tashkent 70000, Uzbekistan. [2].
⁶⁵ 1] Estonian Biocentre, Evolutionary Biology group, Tartu, 51010, Estonia. [2] Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences of Armenia, Yerevan 0014, Armenia.
⁶⁶ 1] Department of Forensic Medicine, Hjelt Institute, University of Helsinki, Helsinki 00014, Finland. [2] Institute of Applied Genetics, Department of Molecular and Medical Genetics, University of North Texas Health Science Center, Fort Worth, Texas 76107, USA.
⁶⁷ 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 15872, Spain.
⁶⁸ Research Fellow, Henry Stewart Group, Russell House, London WC1A 2HN, UK.
⁶⁹ Institute of Bioorganic Chemistry Academy of Sciences Republic of Uzbekistan, Tashkent 100125, Uzbekistan.
⁷⁰ Department of Genetics and Cytology, V. N. Karazin Kharkiv National University, Kharkiv 61077, Ukraine.
⁷¹ 1] Instituto Boliviano de Biología de la Altura, Universidad Mayor de San Andrés, 591 2 La Paz, Bolivia. [2] UniversidadAutonoma Tomás Frías, Potosí, Bolivia.
⁷² 1] Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia. [2] Institute of Internal Medicine, Siberian Branch of Russian Academy of Medical Sciences, Novosibirsk 630089, Russia. [3] Novosibirsk State University, Novosibirsk 630090, Russia.
⁷³ Basic Research Laboratory, NCI, NIH, Frederick National Laboratory, Leidos Biomedical, Frederick, Maryland 21702, USA.
⁷⁴ Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences of Armenia, Yerevan 0014, Armenia.
⁷⁵ 1] Lebanese American University, School of Medicine, Beirut 13-5053, Lebanon. [2] Harvard School of Public Health, Boston, Massachusetts 02115, USA.
⁷⁶ Department of Medical Biology, University of Split, School of Medicine, Split 21000, Croatia.
⁷⁷ Department of Zoology, University of Oxford, Oxford OX1 3PS, UK.
⁷⁸ Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK.
⁷⁹ Department of Biology and Genetics, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
⁸⁰ 1] CSIR-Centre for Cellular and Molecular Biology, Hyderabad 500 007, India. [2] Amgen, 33 Kazantzaki Str, Ilioupolis 16342, Athens, Greece (T.L.); Banaras Hindu University, Varanasi 221 005, India (L.S.).
⁸¹ CSIR-Centre for Cellular and Molecular Biology, Hyderabad 500 007, India.
⁸² 1] Estonian Biocentre, Evolutionary Biology group, Tartu, 51010, Estonia. [2] Department of Evolutionary Biology, University of Tartu, Tartu 51010, Estonia. [3] Estonian Academy of Sciences, Tallinn 10130, Estonia.
⁸³ Institut de Biologia Evolutiva (CSIC-UPF), Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona 08003, Spain.
⁸⁴ 1] Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA. [2] Howard Hughes Medical Institute, University of Washington, Seattle, Washington 98195, USA.
⁸⁵ 1] Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA. [2] Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA. [3] Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts 02115, USA.
⁸⁶ 1] Institute for Archaeological Sciences, University of Tübingen, Tübingen 72074, Germany. [2] Senckenberg Centre for Human Evolution and Palaeoenvironment, University of Tübingen, 72070 Tübingen, Germany. [3] Max Planck Institut für Geschichte und Naturwissenschaften, Jena 07745, Germany.

PMID: 25230663
PMCID: PMC4170574
DOI: 10.1038/nature13673

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

Iosif Lazaridis et al. Nature. 2014.

. 2014 Sep 18;513(7518):409-13.

doi: 10.1038/nature13673.

Authors

Affiliations

¹ 1] Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA. [2] Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA.
² Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA.
³ Institute for Archaeological Sciences, University of Tübingen, Tübingen 72074, Germany.
⁴ Max Planck Institute for Evolutionary Anthropology, Leipzig 04103, Germany.
⁵ Institute of Anthropology, Johannes Gutenberg University Mainz, Mainz D-55128, Germany.
⁶ Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA.
⁷ 1] Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA. [2] Department of Integrative Biology, University of California, Berkeley, California 94720-3140, USA.
⁸ Department of Mathematics and Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
⁹ 1] Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA. [2] Department of Mathematics and Computer Science and Artificial Intelligence Laboratory, Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, USA.
¹⁰ Archaeological Research Laboratory, Stockholm University, 114 18, Sweden.
¹¹ 1] Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA. [2] Max Planck Institute for Evolutionary Anthropology, Leipzig 04103, Germany. [3] Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, IVPP, CAS, Beijing 100049, China.
¹² Australian Centre for Ancient DNA and Environment Institute, School of Earth and Environmental Sciences, University of Adelaide, Adelaide, South Australia 5005, Australia.
¹³ The Cultural Heritage Foundation, Västerås 722 12, Sweden.
¹⁴ 1] National Museum of Natural History, L-2160, Luxembourg. [2] National Center of Archaeological Research, National Museum of History and Art, L-2345, Luxembourg.
¹⁵ Department of Paleoanthropology, Senckenberg Center for Human Evolution and Paleoenvironment, University of Tübingen, Tübingen D-72070, Germany.
¹⁶ National Museum of Natural History, L-2160, Luxembourg.
¹⁷ State Office for Cultural Heritage Management Baden-Württemberg, Osteology, Konstanz D-78467, Germany.
¹⁸ Center for Global Health and Child Development, Kisumu 40100, Kenya.
¹⁹ 1] Institutes of Evolution, Immunology and Infection Research, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3JT, UK. [2] Biochemistry Department, Faculty of Medicine, Sultan Qaboos University, Alkhod, Muscat 123, Oman.
²⁰ Laboratorio de Genética Molecular Poblacional, Instituto Multidisciplinario de Biología Celular (IMBICE), CCT-CONICET &CICPBA, La Plata, B1906APO, Argentina.
²¹ Research Centre for Medical Genetics, Moscow 115478, Russia.
²² 1] Research Centre for Medical Genetics, Moscow 115478, Russia. [2] Vavilov Institute for General Genetics, Moscow 119991, Russia.
²³ Escuela de Biología, Universidad de Costa Rica, San José 2060, Costa Rica.
²⁴ Institute of Biology, Research group GENMOL, Universidad de Antioquia, Medellín, Colombia.
²⁵ Rambam Health Care Campus, Haifa 31096, Israel.
²⁶ Department of Medical Genetics and Szentagothai Research Center, University of Pécs, Pécs H-7624, Hungary.
²⁷ Al Akhawayn University in Ifrane (AUI), School of Science and Engineering, Ifrane 53000, Morocco.
²⁸ Forensic Genetics Laboratory, Institute of Legal Medicine, Università Cattolica del Sacro Cuore, Rome 00168, Italy.
²⁹ 1] Department of Zoology, University of Oxford, Oxford OX1 3PS, UK. [2] Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, UK.
³⁰ Laboratorio di Genetica Molecolare, IRCCS Associazione Oasi Maria SS, Troina 94018, Italy.
³¹ Belgorod State University, Belgorod 308015, Russia.
³² Department of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, Ontario M5G 1L5, Canada.
³³ Servicio de Huellas Digitales Genéticas, School of Pharmacy and Biochemistry, Universidad de Buenos Aires, 1113 CABA, Argentina.
³⁴ Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia.
³⁵ Institute of Linguistics, University of Bern, Bern CH-3012, Switzerland.
³⁶ Laboratory of Human Molecular Genetics, Institute of Molecular and Cellular Biology, Russian Academy of Science, Siberian Branch, Novosibirsk 630090, Russia.
³⁷ Anthropologie Moléculaire et Imagerie de Synthèse, CNRS UMR 5288, Université Paul Sabatier Toulouse III, Toulouse 31000, France.
³⁸ North-Eastern Federal University and Yakut Research Center of Complex Medical Problems, Yakutsk 677013, Russia.
³⁹ Department of Human Genetics, University of Chicago, Chicago, Illinois 60637, USA.
⁴⁰ ARL Division of Biotechnology, University of Arizona, Tucson, Arizona 85721, USA.
⁴¹ Department of Ecology and Evolution, Stony Brook University, Stony Brook, New York 11794, USA.
⁴² Department of Clinical Science, University of Bergen, Bergen 5021, Norway.
⁴³ NextBio, Illumina, Santa Clara, California 95050, USA.
⁴⁴ Department of Medical Genetics, National Human Genome Center, Medical University Sofia, Sofia 1431, Bulgaria.
⁴⁵ 1] Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa 450054, Russia. [2] Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa 450074, Russia.
⁴⁶ College of Medicine, University of Arizona, Tucson, Arizona 85724, USA.
⁴⁷ Division of Biological Anthropology, University of Cambridge, Cambridge CB2 1QH, UK.
⁴⁸ Department of Integrative Biology, University of California, Berkeley, California 94720-3140, USA.
⁴⁹ Department of Human and Medical Genetics, Vilnius University, Vilnius LT-08661, Lithuania.
⁵⁰ Estonian Biocentre, Evolutionary Biology group, Tartu, 51010, Estonia.
⁵¹ Translational Medicine and Neurogenetics, Institut de Génétique et de Biologie Moléculaire et Cellulaire, Illkirch 67404, France.
⁵² 1] Institute of Biochemistry and Genetics, Ufa Research Centre, Russian Academy of Sciences, Ufa 450054, Russia. [2] Department of Genetics and Fundamental Medicine, Bashkir State University, Ufa 450074, Russia. [3] Estonian Biocentre, Evolutionary Biology group, Tartu, 51010, Estonia.
⁵³ 1] Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK. [2] Amgen, 33 Kazantzaki Str, Ilioupolis 16342, Athens, Greece (T.L.); Banaras Hindu University, Varanasi 221 005, India (L.S.).
⁵⁴ Gladstone Institutes, San Francisco, California 94158, USA.
⁵⁵ Department of Evolutionary Biology, University of Tartu, Tartu 51010, Estonia.
⁵⁶ Centro de Investigaciones Biomédicas de Guatemala, Ciudad de Guatemala, Guatemala.
⁵⁷ Research Department, 23andMe, Mountain View, California 94043, USA.
⁵⁸ Cultural Anthropology Program, University of Oulu, Oulu 90014, Finland.
⁵⁹ Department of Biochemistry, Muhimbili University of Health and Allied Sciences, Dar es Salaam 65001, Tanzania.
⁶⁰ Research Institute of Health, North-Eastern Federal University, Yakutsk 677000, Russia.
⁶¹ Dipartimento di Fisica e Chimica, Università di Palermo, Palermo 90128, Italy.
⁶² 1] Instituto de Alta Investigación, Universidad de Tarapacá, Arica 1000000, Chile. [2] Programa de Genética Humana ICBM Facultad de Medicina Universidad de Chile, Santiago 8320000, Chile. [3] Centro de Investigaciones del Hombre en el Desierto, Arica 1000000, Chile.
⁶³ Centre for Population Health Sciences, The University of Edinburgh Medical School, Edinburgh EH8 9AG, UK.
⁶⁴ 1] Institute of Immunology, Academy of Science, Tashkent 70000, Uzbekistan. [2].
⁶⁵ 1] Estonian Biocentre, Evolutionary Biology group, Tartu, 51010, Estonia. [2] Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences of Armenia, Yerevan 0014, Armenia.
⁶⁶ 1] Department of Forensic Medicine, Hjelt Institute, University of Helsinki, Helsinki 00014, Finland. [2] Institute of Applied Genetics, Department of Molecular and Medical Genetics, University of North Texas Health Science Center, Fort Worth, Texas 76107, USA.
⁶⁷ 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 15872, Spain.
⁶⁸ Research Fellow, Henry Stewart Group, Russell House, London WC1A 2HN, UK.
⁶⁹ Institute of Bioorganic Chemistry Academy of Sciences Republic of Uzbekistan, Tashkent 100125, Uzbekistan.
⁷⁰ Department of Genetics and Cytology, V. N. Karazin Kharkiv National University, Kharkiv 61077, Ukraine.
⁷¹ 1] Instituto Boliviano de Biología de la Altura, Universidad Mayor de San Andrés, 591 2 La Paz, Bolivia. [2] UniversidadAutonoma Tomás Frías, Potosí, Bolivia.
⁷² 1] Institute of Cytology and Genetics, Siberian Branch of Russian Academy of Sciences, Novosibirsk 630090, Russia. [2] Institute of Internal Medicine, Siberian Branch of Russian Academy of Medical Sciences, Novosibirsk 630089, Russia. [3] Novosibirsk State University, Novosibirsk 630090, Russia.
⁷³ Basic Research Laboratory, NCI, NIH, Frederick National Laboratory, Leidos Biomedical, Frederick, Maryland 21702, USA.
⁷⁴ Laboratory of Ethnogenomics, Institute of Molecular Biology, National Academy of Sciences of Armenia, Yerevan 0014, Armenia.
⁷⁵ 1] Lebanese American University, School of Medicine, Beirut 13-5053, Lebanon. [2] Harvard School of Public Health, Boston, Massachusetts 02115, USA.
⁷⁶ Department of Medical Biology, University of Split, School of Medicine, Split 21000, Croatia.
⁷⁷ Department of Zoology, University of Oxford, Oxford OX1 3PS, UK.
⁷⁸ Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK.
⁷⁹ Department of Biology and Genetics, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
⁸⁰ 1] CSIR-Centre for Cellular and Molecular Biology, Hyderabad 500 007, India. [2] Amgen, 33 Kazantzaki Str, Ilioupolis 16342, Athens, Greece (T.L.); Banaras Hindu University, Varanasi 221 005, India (L.S.).
⁸¹ CSIR-Centre for Cellular and Molecular Biology, Hyderabad 500 007, India.
⁸² 1] Estonian Biocentre, Evolutionary Biology group, Tartu, 51010, Estonia. [2] Department of Evolutionary Biology, University of Tartu, Tartu 51010, Estonia. [3] Estonian Academy of Sciences, Tallinn 10130, Estonia.
⁸³ Institut de Biologia Evolutiva (CSIC-UPF), Departament de Ciències Experimentals i de la Salut, Universitat Pompeu Fabra, Barcelona 08003, Spain.
⁸⁴ 1] Department of Genome Sciences, University of Washington, Seattle, Washington 98195, USA. [2] Howard Hughes Medical Institute, University of Washington, Seattle, Washington 98195, USA.
⁸⁵ 1] Department of Genetics, Harvard Medical School, Boston, Massachusetts 02115, USA. [2] Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA. [3] Howard Hughes Medical Institute, Harvard Medical School, Boston, Massachusetts 02115, USA.
⁸⁶ 1] Institute for Archaeological Sciences, University of Tübingen, Tübingen 72074, Germany. [2] Senckenberg Centre for Human Evolution and Palaeoenvironment, University of Tübingen, 72070 Tübingen, Germany. [3] Max Planck Institut für Geschichte und Naturwissenschaften, Jena 07745, Germany.

PMID: 25230663
PMCID: PMC4170574
DOI: 10.1038/nature13673

Abstract

We sequenced the genomes of a ∼7,000-year-old farmer from Germany and eight ∼8,000-year-old hunter-gatherers from Luxembourg and Sweden. We analysed these and other ancient genomes with 2,345 contemporary humans to show that most present-day Europeans derive from at least three highly differentiated populations: west European hunter-gatherers, who contributed ancestry to all Europeans but not to Near Easterners; ancient north Eurasians related to Upper Palaeolithic Siberians, who contributed to both Europeans and Near Easterners; and early European farmers, who were mainly of Near Eastern origin but also harboured west European hunter-gatherer related ancestry. We model these populations' deep relationships and show that early European farmers had ∼44% ancestry from a 'basal Eurasian' population that split before the diversification of other non-African lineages.

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Conflict of interest statement

The authors declare competing financial interests: UH is an employee of Illumina, TL is an employee of AMGEN, and JM is an employee of 23andMe.

Figures

**Extended Data Figure 1**
Photographs of analyzed ancient samples. (A) Loschbour skull; (B) Stuttgart skull, missing the lower right M2 we sampled; (C) excavation at Kanaljorden in Motala, Sweden; (D) Motala 1 in situ.

**Extended Data Figure 2**
Pairwise Sequential Markovian Coalescent (PSMC) analysis. (A) Inference of population size as a function of time, showing a very small recent population size over the most recent period in the ancestry of Loschbour (at least the last 5–10 thousand years). (B) Inferred time since the most recent common ancestor from the PSMC for chromosomes 20, 21, 22 (top to bottom); Stuttgart is plotted on top and Loschbour at bottom.

**Extended Data Figure 3**
ADMIXTURE analysis (K=2 to K=20). Ancient samples (Loschbour, Stuttgart, Motala_merge, Motala12, MA1, and LaBrana) are at left.

**Extended Data Figure 4**
ANE ancestry is present in both Europe and the Near East but WHG ancestry is restricted to Europe, which cannot be due to a single admixture event. (x-axis) We computed the statistic *f₄(Test, Stuttgart; MA1, Chimp)*, which measures where MA1 shares more alleles with a test population than with Stuttgart. It is positive for most European and Near Eastern populations, consistent with ANE (MA1-related) gene flow into both regions. (y-axis) We computed the statistic *f₄(Test, Stuttgart; Loschbour, Chimp),* which measures whether Loschbour shares more alleles with a test sample than with Stuttgart. Only European populations show positive values of this statistic, providing evidence of WHG (Loschbour-related) admixture only in Europeans.

**Extended Data Figure 5**
MA1 is the best surrogate for ANE for which we have data. Europeans share more alleles with MA1 than with Karitiana, as we see from the fact that in a plot of *f₄(Test, BedouinB; MA1, Chimp)* and *f₄(Test, BedouinB; Karitiana, Chimp)*, the European cline deviates in the direction of MA1, rather than Karitiana (the slope is >1 and European populations are above the line indicating equality of these two statistics).

**Extended Data Figure 6**
The differential relatedness of West Eurasians to Stuttgart (EEF), Loschbour (WHG), and MA1 (ANE) cannot be explained by two-way mixture. We plot on a West Eurasian map the statistic *f₄(Test, Chimp; A₁, A₂)*, where A₁ and A₂ are a pair of the three ancient samples representing the three ancestral populations of Europe. (A) In both Europe and the Near East/Caucasus, populations from the south have more relatedness to Stuttgart than those from the north where ANE influence is also important. (B) Northern European populations share more alleles with Loschbour than with Stuttgart, as they have additional WHG ancestry beyond what was already present in EEF. (C) We observe a striking contrast between Europe west of the Caucasus and the Near East in degree of relatedness to WHG. In Europe, there is a much higher degree of allele sharing with Loschbour than with MA1, which we ascribe to the 60–80% WHG/(WHG+ANE) ratio in most Europeans that we report in SI14. In contrast, the Near East has no appreciable WHG ancestry but some ANE ancestry, especially in the northern Caucasus. (Jewish populations are marked with a square in this figure to assist in interpretation as their ancestry is often anomalous for their geographic regions.)

**Extended Data Figure 7**
Evidence for Siberian gene flow into far northeastern Europe. Some northeastern European populations (Chuvash, Finnish, Russian, Mordovian, Saami) share more alleles with Han Chinese than with other Europeans who are arrayed in a cline from Stuttgart to Lithuanians/Estonians in a plot of *f₄(Test, BedouinB; Han, Mbuti)* against *f₄(Test, BedouinB; MA1, Mbuti)*.

**Figure 1. Map of West Eurasian populations and Principal Component Analysis**
(a) Geographical locations of analyzed samples, with color coding matching the PCA. We show all sampling locations for each population, which results in multiple points for some (e.g., Spain). (b) PCA on all present-day West Eurasians, with ancient and selected eastern non-African samples projected. European hunter-gatherers fall beyond present-day Europeans in the direction of European differentiation from the Near East. Stuttgart clusters with other Neolithic Europeans and present-day Sardinians. MA1 falls outside the variation of present-day West Eurasians in the direction of southern-northern differentiation along dimension 2.

**Figure 2. Modeling of West Eurasian population history**
(a) A three-way mixture model that is a fit to the data for many populations. Present-day samples are colored in blue, ancient in red, and reconstructed ancestral populations in green. Solid lines represent descent without mixture, and dashed lines represent admixture. We print mixture proportions and one standard error for the two mixtures relating the highly divergent ancestral populations. (We do not print the estimate for the “European” population as it varies depending on the population). (b) We plot the proportions of ancestry from each of three inferred ancestral populations (EEF, ANE and WHG).

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References

1. Keller A, et al. New insights into the Tyrolean Iceman’s origin and phenotype as inferred by whole-genome sequencing. Nat Commun. 2012;3:698. - PubMed
1. Olalde I, et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature. 2014;507:225–228. - PMC - PubMed
1. Raghavan M, et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature. 2014;505:87–91. - PMC - PubMed
1. Skoglund P, et al. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science. 2012;336:466–469. - PubMed
1. Bramanti B, et al. Genetic discontinuity between local hunter-gatherers and Central Europe’s first farmers. Science. 2009;326:137–140. - PubMed

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[1] Keller A, et al. New insights into the Tyrolean Iceman’s origin and phenotype as inferred by whole-genome sequencing. Nat Commun. 2012;3:698. - PubMed

[2] Keller A, et al. New insights into the Tyrolean Iceman’s origin and phenotype as inferred by whole-genome sequencing. Nat Commun. 2012;3:698. - PubMed

[3] Olalde I, et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature. 2014;507:225–228. - PMC - PubMed

[4] Olalde I, et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature. 2014;507:225–228. - PMC - PubMed

[5] Raghavan M, et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature. 2014;505:87–91. - PMC - PubMed

[6] Raghavan M, et al. Upper Palaeolithic Siberian genome reveals dual ancestry of Native Americans. Nature. 2014;505:87–91. - PMC - PubMed

[7] Skoglund P, et al. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science. 2012;336:466–469. - PubMed

[8] Skoglund P, et al. Origins and genetic legacy of Neolithic farmers and hunter-gatherers in Europe. Science. 2012;336:466–469. - PubMed

[9] Bramanti B, et al. Genetic discontinuity between local hunter-gatherers and Central Europe’s first farmers. Science. 2009;326:137–140. - PubMed

[10] Bramanti B, et al. Genetic discontinuity between local hunter-gatherers and Central Europe’s first farmers. Science. 2009;326:137–140. - PubMed

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

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

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