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      Parallel paleogenomic transects reveal complex genetic history of early European farmers

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      1 , 2 , 1 , 3 , 2 , 2 , 4 , 1 , 1 , 5 , 1 , 5 , 1 , 5 , 1 , 5 , 1 , 5 , 1 , 5 , 1 , 6 , 2 , 2 , 2 , 2 , 2 , 2 , 2 , 7 , 7 , 8 , 8 , 9 , 9 , 9 , 10 , 11 , 12 , 2 , 13 , 14 , 14 , 15 , 15 , 16 , 17 , 18 , 19 , 18 , 20 , 18 , 20 , 21 , 22 , 22 , 23 , 23 , 4 , 24 , 25 , 26 , 27 , 6 , 28 , 4 , 2 , 29 , 30 , 31 , 6 , 32 , 1 , 3 , 5
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          Abstract

          Ancient DNA studies have established that Neolithic European populations were descended from Anatolian migrants 18 who received a limited amount of admixture from resident hunter-gatherers 35, 9 . Many open questions remain, however, about the spatial and temporal dynamics of population interactions and admixture during the Neolithic period. Using the highest-resolution genome-wide ancient DNA data set assembled to date—a total of 180 samples, 130 newly reported here, from the Neolithic and Chalcolithic of Hungary (6000–2900 BCE, n = 100), Germany (5500–3000 BCE, n = 42), and Spain (5500–2200 BCE, n = 38)—we investigate the population dynamics of Neolithization across Europe. We find that genetic diversity was shaped predominantly by local processes, with varied sources and proportions of hunter-gatherer ancestry among the three regions and through time. Admixture between groups with different ancestry profiles was pervasive and resulted in observable population transformation across almost all cultural transitions. Our results shed new light on the ways that gene flow reshaped European populations throughout the Neolithic period and demonstrate the potential of time-series-based sampling and modeling approaches to elucidate multiple dimensions of historical population interactions.

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          Most cited references38

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

          We sequenced genomes from a $\sim$7,000 year old early farmer from Stuttgart in Germany, an $\sim$8,000 year old hunter-gatherer from Luxembourg, and seven $\sim$8,000 year old hunter-gatherers from southern Sweden. We analyzed these data together with other ancient genomes and 2,345 contemporary humans to show that the great majority of present-day Europeans derive from at least three highly differentiated populations: West European Hunter-Gatherers (WHG), who contributed ancestry to all Europeans but not to Near Easterners; Ancient North Eurasians (ANE), who were most closely related to Upper Paleolithic Siberians and contributed to both Europeans and Near Easterners; and Early European Farmers (EEF), who were mainly of Near Eastern origin but also harbored WHG-related ancestry. We model these populations' deep relationships and show that EEF had $\sim$44% ancestry from a "Basal Eurasian" lineage that split prior to the diversification of all other non-African lineages.
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            Genomic insights into the origin of farming in the ancient Near East

            We report genome-wide ancient DNA from 44 ancient Near Easterners ranging in time between ~12,000-1,400 BCE, from Natufian hunter-gatherers to Bronze Age farmers. We show that the earliest populations of the Near East derived around half their ancestry from a ‘Basal Eurasian’ lineage that had little if any Neanderthal admixture and that separated from other non-African lineages prior to their separation from each other. The first farmers of the southern Levant (Israel and Jordan) and Zagros Mountains (Iran) were strongly genetically differentiated, and each descended from local hunter-gatherers. By the time of the Bronze Age, these two populations and Anatolian-related farmers had mixed with each other and with the hunter-gatherers of Europe to drastically reduce genetic differentiation. The impact of the Near Eastern farmers extended beyond the Near East: farmers related to those of Anatolia spread westward into Europe; farmers related to those of the Levant spread southward into East Africa; farmers related to those from Iran spread northward into the Eurasian steppe; and people related to both the early farmers of Iran and to the pastoralists of the Eurasian steppe spread eastward into South Asia.
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              The genetic history of Ice Age Europe

              Modern humans arrived in Europe ~45,000 years ago, but little is known about their genetic composition before the start of farming ~8,500 years ago. We analyze genome-wide data from 51 Eurasians from ~45,000-7,000 years ago. Over this time, the proportion of Neanderthal DNA decreased from 3–6% to around 2%, consistent with natural selection against Neanderthal variants in modern humans. Whereas the earliest modern humans in Europe did not contribute substantially to present-day Europeans, all individuals between ~37,000 and ~14,000 years ago descended from a single founder population which forms part of the ancestry of present-day Europeans. A ~35,000 year old individual from northwest Europe represents an early branch of this founder population which was then displaced across a broad region, before reappearing in southwest Europe during the Ice Age ~19,000 years ago. During the major warming period after ~14,000 years ago, a new genetic component related to present-day Near Easterners appears in Europe. These results document how population turnover and migration have been recurring themes of European pre-history.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                9 October 2017
                08 November 2017
                16 November 2017
                29 May 2018
                : 551
                : 7680
                : 368-372
                Affiliations
                [1 ]Department of Genetics, Harvard Medical School, Boston, MA 02115, USA
                [2 ]Institute of Archaeology, Research Centre for the Humanities, Hungarian Academy of Sciences, Budapest H-1097, Hungary
                [3 ]Medical and Population Genetics Program, Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA
                [4 ]Institute of Organimsic and Molecular Evolution, Johannes Gutenberg University Mainz, Mainz D-55128, Germany
                [5 ]Howard Hughes Medical Institute, Harvard Medical School, Boston, MA 02115, USA
                [6 ]Australian Centre for Ancient DNA, School of Biological Sciences, University of Adelaide, Adelaide, SA 5005, Australia
                [7 ]Móra Ferenc Museum, H-6720 Szeged, Hungary
                [8 ]Herman Ottó Museum, H-3529 Miskolc, Hungary
                [9 ]Institute of Archaeological Sciences, Eötvös Loránd University, Budapest H-1088, Hungary
                [10 ]Laczkó Dezső Museum, H-8200 Veszprém, Hungary
                [11 ]Balaton Museum, H-8360 Keszthely, Hungary
                [12 ]Department of Archaeological Excavations and Artefact Processing, Hungarian National Museum, Budapest H-1088, Hungary
                [13 ]Jósa András Museum, H-4400 Nyíregyháza, Hungary
                [14 ]Déri Museum, H-4026 Debrecen, Hungary
                [15 ]Department of Biological Anthropology, Szeged University, H-6726 Szeged, Hungary
                [16 ]Department of Biochemistry and Medical Chemistry, University of Pécs, Pécs H-7624, Hungary
                [17 ]Imaging Center for Life and Material Sciences, University of Pécs, Pécs H-7624, Hungary
                [18 ]Szentágothai Research Center, University of Pécs, Pécs H-7624, Hungary
                [19 ]PTE-MTA Human Reproduction Research Group, Pécs H-7624, Hungary
                [20 ]Department of Medical Genetics and Szentágothai Research Center, University of Pécs, Pécs H-7624, Hungary
                [21 ]Dobó István Castle Museum, Eger H-3300, Hungary
                [22 ]Department of Geography, Prehistory, and Archaeology, University of the Basque Country, Investigation Group IT622-13, 01006 Vitoria-Gasteiz, Spain
                [23 ]CRONOS SC, 09007 Burgos, Spain
                [24 ]Department of Prehistoric Archaeology, Free University of Berlin, 14195 Berlin, Germany
                [25 ]Curt-Engelhorn-Centre Archaeometry gGmbH, 68159 Mannheim, Germany
                [26 ]Commission for Westphalian Antiquities, Westphalia-Lippe Regional Association, 48157 Münster, Germany
                [27 ]State Office for Heritage Management and Archaeology Saxony-Anhalt and State Heritage Museum, D-06114 Halle, Germany
                [28 ]Environment Institute, University of Adelaide, Adelaide, SA 5005, Australia
                [29 ]Romano-Germanic Commission, German Archaeological Institute, D-60325 Frankfurt am Main, Germany
                [30 ]Center of Natural and Cultural History of Man, Danube Private University, A-3500 Krems-Stein, Austria
                [31 ]Institute of Evolutionary Biology (CSIC-UPF), 08003 Barcelona, Spain
                [32 ]Department of Archaeogenetics, Max Planck Institute for the Science of Human History, 07745 Jena, Germany
                Author notes
                [* ]Correspondence and requests for materials should be addressed to M.L. ( mlipson@ 123456genetics.med.harvard.edu ), A.S.-N. ( szecsenyi-nagy.anna@ 123456btk.mta.hu ), or D.R. ( reich@ 123456genetics.med.harvard.edu )
                [†]

                These authors contributed equally to this work

                Article
                NIHMS911574
                10.1038/nature24476
                5973800
                29144465
                e4705187-eecd-4ad6-9e36-2dd1be74428d

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