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      Palaeogenomics of Upper Palaeolithic to Neolithic European hunter-gatherers

      research-article
      1 , 2 , 3 , , 3 , 4 , , 3 , 3 , 5 , 6 , 3 , 3 , 3 , 7 , 3 , 3 , 8 , 3 , 9 , 3 , 3 , 10 , 3 , 11 , 2 , 12 , 12 , 12 , 13 , 13 , 14 , 15 , 13 , 16 , 17 , 18 , 18 , 19 , 6 , 20 , 21 , 22 , 6 , 20 , 23 , 24 , 25 , 26 , 27 , 28 , 27 , 28 , 29 , 6 , 6 , 30 , 6 , 31 , 31 , 32 , 19 , 19 , 19 , 33 , 34 , 35 , 15 , 36 , 37 , 38 , 39 , 39 , 40 , 41 , 41 , 42 , 43 , 44 , 45 , 46 , 6 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 55 , 57 , 57 , 27 , 58 , 58 , 59 , 60 , 60 , 60 , 61 , 62 , 55 , 63 , 23 , 64 , 65 , 66 , 31 , 31 , 67 , 68 , 69 , 70 , 2 , 71 , 2 , 71 , 38 , 58 , 72 , 73 , 73 , 74 , 19 , 75 , 19 , 37 , 76 , 76 , 77 , 78 , 79 , 80 , 81 , 81 , 82 , 83 , 61 , 84 , 85 , 86 , 87 , 88 , 87 , 89 , 89 , 90 , 91 , 2 , 92 , 19 , 2 , 93 , 94 , 95 , 96 , 97 , 98 , 99 , 100 , 54 , 101 , 102 , 11 , 103 , 3 , 3 ,
      Nature
      Nature Publishing Group UK
      Archaeology, Population genetics, Biological anthropology, Evolutionary genetics

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          Abstract

          Modern humans have populated Europe for more than 45,000 years 1, 2 . Our knowledge of the genetic relatedness and structure of ancient hunter-gatherers is however limited, owing to the scarceness and poor molecular preservation of human remains from that period 3 . Here we analyse 356 ancient hunter-gatherer genomes, including new genomic data for 116 individuals from 14 countries in western and central Eurasia, spanning between 35,000 and 5,000 years ago. We identify a genetic ancestry profile in individuals associated with Upper Palaeolithic Gravettian assemblages from western Europe that is distinct from contemporaneous groups related to this archaeological culture in central and southern Europe 4 , but resembles that of preceding individuals associated with the Aurignacian culture. This ancestry profile survived during the Last Glacial Maximum (25,000 to 19,000 years ago) in human populations from southwestern Europe associated with the Solutrean culture, and with the following Magdalenian culture that re-expanded northeastward after the Last Glacial Maximum. Conversely, we reveal a genetic turnover in southern Europe suggesting a local replacement of human groups around the time of the Last Glacial Maximum, accompanied by a north-to-south dispersal of populations associated with the Epigravettian culture. From at least 14,000 years ago, an ancestry related to this culture spread from the south across the rest of Europe, largely replacing the Magdalenian-associated gene pool. After a period of limited admixture that spanned the beginning of the Mesolithic, we find genetic interactions between western and eastern European hunter-gatherers, who were also characterized by marked differences in phenotypically relevant variants.

          Abstract

          Combined analysis of new genomic data from 116 ancient hunter-gatherer individuals together with previously published data provides insights into the genetic structure and demographic shifts of west Eurasian forager populations over a period of 30,000 years.

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          The Sequence Alignment/Map format and SAMtools

          Summary: The Sequence Alignment/Map (SAM) format is a generic alignment format for storing read alignments against reference sequences, supporting short and long reads (up to 128 Mbp) produced by different sequencing platforms. It is flexible in style, compact in size, efficient in random access and is the format in which alignments from the 1000 Genomes Project are released. SAMtools implements various utilities for post-processing alignments in the SAM format, such as indexing, variant caller and alignment viewer, and thus provides universal tools for processing read alignments. Availability: http://samtools.sourceforge.net Contact: rd@sanger.ac.uk
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            Fast and accurate short read alignment with Burrows–Wheeler transform

            Motivation: The enormous amount of short reads generated by the new DNA sequencing technologies call for the development of fast and accurate read alignment programs. A first generation of hash table-based methods has been developed, including MAQ, which is accurate, feature rich and fast enough to align short reads from a single individual. However, MAQ does not support gapped alignment for single-end reads, which makes it unsuitable for alignment of longer reads where indels may occur frequently. The speed of MAQ is also a concern when the alignment is scaled up to the resequencing of hundreds of individuals. Results: We implemented Burrows-Wheeler Alignment tool (BWA), a new read alignment package that is based on backward search with Burrows–Wheeler Transform (BWT), to efficiently align short sequencing reads against a large reference sequence such as the human genome, allowing mismatches and gaps. BWA supports both base space reads, e.g. from Illumina sequencing machines, and color space reads from AB SOLiD machines. Evaluations on both simulated and real data suggest that BWA is ∼10–20× faster than MAQ, while achieving similar accuracy. In addition, BWA outputs alignment in the new standard SAM (Sequence Alignment/Map) format. Variant calling and other downstream analyses after the alignment can be achieved with the open source SAMtools software package. Availability: http://maq.sourceforge.net Contact: rd@sanger.ac.uk
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              MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms.

              The Molecular Evolutionary Genetics Analysis (Mega) software implements many analytical methods and tools for phylogenomics and phylomedicine. Here, we report a transformation of Mega to enable cross-platform use on Microsoft Windows and Linux operating systems. Mega X does not require virtualization or emulation software and provides a uniform user experience across platforms. Mega X has additionally been upgraded to use multiple computing cores for many molecular evolutionary analyses. Mega X is available in two interfaces (graphical and command line) and can be downloaded from www.megasoftware.net free of charge.
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                Author and article information

                Contributors
                cosimo.posth@uni-tuebingen.de
                yuhe@pku.edu.cn
                krause@eva.mpg.de
                Journal
                Nature
                Nature
                Nature
                Nature Publishing Group UK (London )
                0028-0836
                1476-4687
                1 March 2023
                1 March 2023
                2023
                : 615
                : 7950
                : 117-126
                Affiliations
                [1 ]GRID grid.10392.39, ISNI 0000 0001 2190 1447, Archaeo- and Palaeogenetics, Institute for Archaeological Sciences, Department of Geosciences, , University of Tübingen, ; Tübingen, Germany
                [2 ]GRID grid.511394.b, Senckenberg Centre for Human Evolution and Palaeoenvironment at the University of Tübingen, ; Tübingen, Germany
                [3 ]GRID grid.419518.0, ISNI 0000 0001 2159 1813, Department of Archaeogenetics, , Max Planck Institute for Evolutionary Anthropology, ; Leipzig, Germany
                [4 ]GRID grid.11135.37, ISNI 0000 0001 2256 9319, State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, , Peking University, ; Beijing, China
                [5 ]GRID grid.253563.4, ISNI 0000 0001 0657 9381, Department of Anthropology, , California State University Northridge, ; Northridge, CA USA
                [6 ]Université de Bordeaux, CNRS, MC, PACEA UMR 5199, Pessac, France
                [7 ]GRID grid.1010.0, ISNI 0000 0004 1936 7304, School of Mathematical Sciences, , University of Adelaide, ; Adelaide, South Australia Australia
                [8 ]Instituto Universitario de Investigación en Ciencias Ambientales de Aragón, IUCA-Aragosaurus, Zaragoza, Spain
                [9 ]GRID grid.469873.7, ISNI 0000 0004 4914 1197, Department of Archaeogenetics, , Max Planck Institute for the Science of Human History, ; Jena, Germany
                [10 ]GRID grid.9613.d, ISNI 0000 0001 1939 2794, Institute of Zoology and Evolutionary Research, , University of Jena, ; Jena, Germany
                [11 ]GRID grid.77268.3c, ISNI 0000 0004 0543 9688, Center of Excellence ‘Archaeometry’, , Kazan Federal University, ; Kazan, Russia
                [12 ]GRID grid.8404.8, ISNI 0000 0004 1757 2304, Department of Biology, , University of Florence, ; Florence, Italy
                [13 ]GRID grid.10939.32, ISNI 0000 0001 0943 7661, Estonian Biocentre, Institute of Genomics, , University of Tartu, ; Tartu, Estonia
                [14 ]GRID grid.5335.0, ISNI 0000000121885934, St John’s College, , University of Cambridge, ; Cambridge, UK
                [15 ]GRID grid.10776.37, ISNI 0000 0004 1762 5517, Department of Biological, Chemical and Pharmaceutical Sciences and Technologies, , University of Palermo, ; Palermo, Italy
                [16 ]GRID grid.5608.b, ISNI 0000 0004 1757 3470, Department of Biology, , University of Padova, ; Padova, Italy
                [17 ]GRID grid.6292.f, ISNI 0000 0004 1757 1758, Department of Chemistry G. Ciamician, Alma Mater Studiorum, , University of Bologna, ; Bologna, Italy
                [18 ]GRID grid.419518.0, ISNI 0000 0001 2159 1813, Department of Human Evolution, , Max Planck Institute for Evolutionary Anthropology, ; Leipzig, Germany
                [19 ]UMR 8068 CNRS, TEMPS—Technologie et Ethnologie des Mondes Préhistoriques, Nanterre Cedex, France
                [20 ]Musée National de Préhistoire, Les Eyzies de Tayac, France
                [21 ]Paléotime, Villard-de-Lans, France
                [22 ]GRID grid.440910.8, ISNI 0000 0001 2196 152X, UMR 5140 CNRS, Archéologie des Sociétés Méditerranéennes, , Université Paul-Valéry, ; Montpellier, France
                [23 ]GRID grid.503218.d, ISNI 0000 0004 0383 1918, UMR 7194, Histoire Naturelle de l’Homme Préhistorique (HNHP), Département Homme et Environnement, , Muséum National d’Histoire Naturelle, CNRS, UPVD, ; Paris, France
                [24 ]Association APRAGE (Approches pluridisciplinaires de recherche archéologique du Grand-Est), Besançon, France
                [25 ]Inrap GE, Metz, France
                [26 ]GRID grid.9759.2, ISNI 0000 0001 2232 2818, Skeletal Biology Research Centre, School of Anthropology and Conservation, , University of Kent, ; Canterbury, UK
                [27 ]GRID grid.9024.f, ISNI 0000 0004 1757 4641, Dipartimento di Scienze Fisiche, della Terra e dell’Ambiente, U.R. Preistoria e Antropologia, , Università degli Studi di Siena, ; Siena, Italy
                [28 ]Accademia dei Fisiocritici, Siena, Italy
                [29 ]Centro Studi sul Quaternario ODV, Sansepolcro, Italy
                [30 ]Institut National de Recherches Archéologiques, Bertrange, Luxembourg
                [31 ]GRID grid.6292.f, ISNI 0000 0004 1757 1758, Department of Cultural Heritage, , University of Bologna, ; Ravenna, Italy
                [32 ]GRID grid.4711.3, ISNI 0000 0001 2183 4846, Human Ecology and Archaeology (HUMANE), Department of Archaeology and Anthropology, , Institució Milà i Fontanals de Investigación en Humanidades, Consejo Superior de Investigaciones Científicas (IMF - CSIC), ; Barcelona, Spain
                [33 ]GRID grid.410350.3, ISNI 0000 0001 2174 9334, UMR 7209—Archéozoologie et Archéobotanique-Sociétés, Pratiques et Environnements, Muséum National d’Histoire Naturelle, ; Paris, France
                [34 ]GRID grid.7763.5, ISNI 0000 0004 1755 3242, Dipartimento di Scienze Della Vita e Dell’Ambiente, Sezione di Neuroscienze e Antropologia, , Università Degli Studi di Cagliari, Cittadella Monserrato, ; Cagliari, Italy
                [35 ]GRID grid.5395.a, ISNI 0000 0004 1757 3729, Dipartimento di Civiltà e Forme Del Sapere, , Università di Pisa, ; Pisa, Italy
                [36 ]GRID grid.4830.f, ISNI 0000 0004 0407 1981, Center for Isotope Research, , Groningen University, ; Groningen, The Netherlands
                [37 ]Inrap CIF, Croissy-Beaubourg, France
                [38 ]GRID grid.508487.6, ISNI 0000 0004 7885 7602, UMR 7206 Éco-Anthropologie, Équipe ABBA. CNRS, MNHN, , Université de Paris Cité, Musée de l’Homme, ; Paris, France
                [39 ]GRID grid.11166.31, ISNI 0000 0001 2160 6368, PALEVOPRIM Lab UMR 7262 CNRS-INEE, , University of Poitiers, ; Poitiers, France
                [40 ]GRID grid.11166.31, ISNI 0000 0001 2160 6368, Centre de Valorisation des Collections Scientifiques, , Université de Poitiers, ; Mignaloux Beauvoir, France
                [41 ]Musées de Poitiers–Ville de Poitiers, Poitiers, France
                [42 ]GRID grid.11480.3c, ISNI 0000000121671098, Departamento de Geología, Facultad de Ciencia y Tecnología, , Universidad del País Vasco/Euskal Herriko Unibertsitatea (UPV/EHU), ; Leioa, Spain
                [43 ]Sociedad de Ciencias Aranzadi, Donostia-San Sebastian, Spain
                [44 ]Centro UCM-ISCIII de Investigación sobre Evolución y Comportamiento Humanos, Madrid, Spain
                [45 ]GRID grid.13856.39, ISNI 0000 0001 2154 3176, Institute of Archaeology, , University of Rzeszów, ; Rzeszów, Poland
                [46 ]Foundation for Rzeszów Archaeological Centre, Rzeszów, Poland
                [47 ]GRID grid.32224.35, ISNI 0000 0004 0386 9924, Center for Genomic Medicine, , Massachusetts General Hospital, ; Boston, MA USA
                [48 ]GRID grid.38142.3c, ISNI 000000041936754X, Department of Psychiatry, , Harvard Medical School, ; Boston, MA USA
                [49 ]GRID grid.4830.f, ISNI 0000 0004 0407 1981, Groninger Instituut voor Archeologie, , Groningen University, ; Groningen, The Netherlands
                [50 ]Stralsund Museum, Stralsund, Germany
                [51 ]GRID grid.413454.3, ISNI 0000 0001 1958 0162, Institute of Archaeology and Ethnology, , Polish Academy of Science, ; Poznań, Poland
                [52 ]Institute of History, Archaeology and Ethnography, Dushanbe, Tajikistan
                [53 ]GRID grid.415877.8, ISNI 0000 0001 2254 1834, ArchaeoZOOlogy in Siberia and Central Asia—ZooSCAn, CNRS–IAET SB RAS International Research Laboratory, IRL 2013, , Institute of Archaeology SB RAS, ; Novosibirsk, Russia
                [54 ]GRID grid.14476.30, ISNI 0000 0001 2342 9668, Research Institute and Museum of Anthropology, , Moscow State University, ; Moscow, Russia
                [55 ]GRID grid.7821.c, ISNI 0000 0004 1770 272X, Grupo de I+D+i EVOADAPTA (Evolución Humana y Adaptaciones durante la Prehistoria) Departamento de Ciencias Históricas, , Universidad de Cantabria, ; Santander, Spain
                [56 ]GRID grid.7821.c, ISNI 0000 0004 1770 272X, Instituto Internacional de Investigaciones Prehistóricas de Cantabria (IIIPC), , Universidad de Cantabria-Gobierno de Cantabria-Banco Santander, ; Santander, Spain
                [57 ]GRID grid.10863.3c, ISNI 0000 0001 2164 6351, Departamento de Biología de Organismos y Sistemas, , Universidad de Oviedo, ; Oviedo, Spain
                [58 ]GRID grid.20478.39, ISNI 0000 0001 2171 9581, Quaternary Environments and Humans, OD Earth and History of Life, , Royal Belgian Institute of Natural Sciences, ; Brussels, Belgium
                [59 ]GRID grid.425641.0, ISNI 0000 0001 2342 957X, Musées Royaux d’Art et d’Histoire, ; Bruxelles, Belgium
                [60 ]GRID grid.5319.e, ISNI 0000 0001 2179 7512, Institute of Historical Research, , University of Girona, ; Catalonia, Spain
                [61 ]INRAP/UMR 8215 Trajectoires 21, Paris, France
                [62 ]GRID grid.215654.1, ISNI 0000 0001 2151 2636, School of Human Evolution and Social Change, , Arizona State University, ; Tempe, AZ USA
                [63 ]GRID grid.266832.b, ISNI 0000 0001 2188 8502, Department of Anthropology, , University of New Mexico, ; Albuquerque, NM USA
                [64 ]GéoArchPal-GéoArchÉon, Viéville sous-les-Cotes, France
                [65 ]GRID grid.472881.0, ISNI 0000 0001 1348 1753, Archäologie & Münzkabinett, , Universalmuseum Joanneum, ; Graz, Austria
                [66 ]Museum ‘Das Dorf des Welan’, Wöllersdorf-Steinabrückl, Austria
                [67 ]Pradis Cave Museum, Clauzetto, Italy
                [68 ]GRID grid.8484.0, ISNI 0000 0004 1757 2064, Department of Humanities, , University of Ferrara, ; Ferrara, Italy
                [69 ]GRID grid.450218.a, ISNI 0000 0004 1784 7806, National Museum of Antiquities, ; Leiden, The Netherlands
                [70 ]GRID grid.5132.5, ISNI 0000 0001 2312 1970, Faculty of Archaeology, , Leiden University, ; Leiden, The Netherlands
                [71 ]GRID grid.10392.39, ISNI 0000 0001 2190 1447, Biogeology, Department of Geosciences, , University of Tübingen, ; Tübingen, Germany
                [72 ]GRID grid.4861.b, ISNI 0000 0001 0805 7253, Unité de Recherches Art, Archéologie Patrimoine, , Université de Liège, ; Liège, Belgium
                [73 ]GRID grid.5268.9, ISNI 0000 0001 2168 1800, I.U. de Investigación en Arqueología y Patrimonio Histórico, , University of Alicante, Sant Vicent del Raspeig, ; Alicante, Spain
                [74 ]Arpa Patrimonio S. L., Alicante, Spain
                [75 ]GRID grid.7177.6, ISNI 0000000084992262, Amsterdam Centre of Ancient Studies and Archaeology, University of Amsterdam, ; Amsterdam, The Netherlands
                [76 ]GRID grid.6441.7, ISNI 0000 0001 2243 2806, Department of Anatomy, Histology and Anthropology, Faculty of Medicine, , Vilnius University, ; Vilnius, Lithuania
                [77 ]Service Régional de l’Archéologie de Bourgogne-Franche-Comté, Besançon Cedex, France
                [78 ]GRID grid.12366.30, ISNI 0000 0001 2182 6141, Laboratoire de Chrono-Environnement, UMR 6249 du CNRS, UFR des Sciences et Techniques, ; Besançon Cedex, France
                [79 ]Weyhe, Germany
                [80 ]Ulm, Germany
                [81 ]LVR-LandesMuseum Bonn, Bonn, Germany
                [82 ]GRID grid.10392.39, ISNI 0000 0001 2190 1447, Institute of Pre- and Protohistory, , University of Tübingen, ; Tübingen, Germany
                [83 ]Department of Archeological Sciences, Thuringian State Office for Monuments Preservation and Archeology, Weimar, Germany
                [84 ]GRID grid.5100.4, ISNI 0000 0001 2322 497X, University of Bucharest, Faculty of Geology and Geophysics, , Department of Geology, ; Bucharest, Romania
                [85 ]Institute for Advanced Studies in Levant Culture and Civilization, Bucharest, Romania
                [86 ]GRID grid.424195.f, ISNI 0000 0001 2106 6832, German Archaeological Institute, ; Berlin, Germany
                [87 ]Brandenburg Authorities for Heritage Management and Archaeological State Museum, Zossen, Germany
                [88 ]GRID grid.9764.c, ISNI 0000 0001 2153 9986, Institute for Pre- and Protohistory, , Kiel University, ; Kiel, Germany
                [89 ]GRID grid.418095.1, ISNI 0000 0001 1015 3316, Institute of Archeology at Brno, Czech Academy of Sciences, , Centre for Palaeolithic and Paleoanthropology, ; Brno, Czechia
                [90 ]GRID grid.465449.e, ISNI 0000 0001 1214 1108, Institute of Archaeology, , Academy of Sciences of the Republic of Tatarstan, ; Kazan, Russia
                [91 ]GRID grid.445790.b, ISNI 0000 0001 2218 2982, Samara State University of Social Sciences and Education, ; Samara, Russia
                [92 ]GRID grid.10392.39, ISNI 0000 0001 2190 1447, Early Prehistory and Quaternary Ecology, Department of Geosciences, , University of Tübingen, ; Tübingen, Germany
                [93 ]GRID grid.10392.39, ISNI 0000 0001 2190 1447, Paleoanthropology, Institute for Archaeological Sciences, Department of Geosciences, , University of Tübingen, ; Tübingen, Germany
                [94 ]GRID grid.10392.39, ISNI 0000 0001 2190 1447, DFG Centre for Advanced Studies ‘Words, Bones, Genes, Tools’, , University of Tübingen, ; Tübingen, Germany
                [95 ]GRID grid.20478.39, ISNI 0000 0001 2171 9581, Royal Belgian Institute of Natural Sciences, ; Brussels, Belgium
                [96 ]Anthropologie-Büro, Berlin, Germany
                [97 ]GRID grid.4886.2, ISNI 0000 0001 2192 9124, Institute of Archaeology Russian, , Academy of Sciences, ; Moscow, Russia
                [98 ]GRID grid.4991.5, ISNI 0000 0004 1936 8948, School of Archaeology, , University of Oxford, ; Oxford, UK
                [99 ]GRID grid.465399.4, ISNI 0000 0001 2097 4804, Peter the Great Museum of Anthropology and Ethnography (Kunstkamera), Russian Academy of Sciences, ; Saint Petersburg, Russia
                [100 ]GRID grid.7737.4, ISNI 0000 0004 0410 2071, Department of Cultures, , University of Helsinki, ; Helsinki, Finland
                [101 ]GRID grid.7450.6, ISNI 0000 0001 2364 4210, Seminar for Pre- and Protohistory, , Göttingen University, ; Göttingen, Germany
                [102 ]Lower Saxony State Service for Cultural Heritage, Hannover, Germany
                [103 ]GRID grid.10419.3d, ISNI 0000000089452978, Department of Human Genetics, , Leiden University Medical Center, ; Leiden, The Netherlands
                Author information
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                http://orcid.org/0000-0003-1323-4730
                http://orcid.org/0000-0003-0358-0285
                http://orcid.org/0000-0002-4884-9682
                http://orcid.org/0000-0002-4204-5018
                http://orcid.org/0000-0003-3861-8677
                http://orcid.org/0000-0002-9357-5238
                http://orcid.org/0000-0002-5800-3787
                http://orcid.org/0000-0003-2434-2542
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                http://orcid.org/0000-0002-7832-8212
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                http://orcid.org/0000-0003-3844-5147
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                http://orcid.org/0000-0003-2475-2007
                http://orcid.org/0000-0001-9144-3920
                Article
                5726
                10.1038/s41586-023-05726-0
                9977688
                36859578
                a427bfb7-dc58-4507-a394-82b8042a889e
                © The Author(s) 2023

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                History
                : 10 June 2022
                : 12 January 2023
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                archaeology,population genetics,biological anthropology,evolutionary genetics
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                archaeology, population genetics, biological anthropology, evolutionary genetics

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