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      Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe

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      a , b , 2 , b , b , c , d , d , e , f , b , g , h , i , i , j , k , l , m , n , o , p , l , q , r , s , t , p , u , v , w , l , l , x , y , z , u , p , c , aa , bb , cc , dd , ee , ff , gg , hh , x , ii , jj , kk , b , b , ll , mm , nn , oo , pp , qq , mm , rr , ss , tt , uu , vv , ww , xx , x , yy , mm , zz , aaa , f , bbb , ccc , ddd , eee , fff , ggg , hhh , iii , zz , mm , jjj , kkk , lll , mmm , nnn , bbb , mm , ooo , v , y , mm , ppp , qqq , m , rrr , sss , ttt , l , uuu , vvv , www , mm , i , ll , ggg , xxx , d , yyy , zzz , b , 2
      Proceedings of the National Academy of Sciences of the United States of America
      National Academy of Sciences
      domestication, evolution, gene flow, Neolithic

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          Archaeological evidence indicates that domestic pigs arrived in Europe, alongside farmers from the Near East ∼8,500 y ago, yet mitochondrial genomes of modern European pigs are derived from European wild boars. To address this conundrum, we obtained mitochondrial and nuclear data from modern and ancient Near Eastern and European pigs. Our analyses indicate that, aside from a coat color gene, most Near Eastern ancestry in the genomes of European domestic pigs disappeared over 3,000 y as a result of interbreeding with local wild boars. This implies that pigs were not domesticated independently in Europe, yet the first 2,500 y of human-mediated selection applied by Near Eastern Neolithic farmers played little role in the development of modern European pigs.

          Abstract

          Archaeological evidence indicates that pig domestication had begun by ∼10,500 y before the present (BP) in the Near East, and mitochondrial DNA (mtDNA) suggests that pigs arrived in Europe alongside farmers ∼8,500 y BP. A few thousand years after the introduction of Near Eastern pigs into Europe, however, their characteristic mtDNA signature disappeared and was replaced by haplotypes associated with European wild boars. This turnover could be accounted for by substantial gene flow from local European wild boars, although it is also possible that European wild boars were domesticated independently without any genetic contribution from the Near East. To test these hypotheses, we obtained mtDNA sequences from 2,099 modern and ancient pig samples and 63 nuclear ancient genomes from Near Eastern and European pigs. Our analyses revealed that European domestic pigs dating from 7,100 to 6,000 y BP possessed both Near Eastern and European nuclear ancestry, while later pigs possessed no more than 4% Near Eastern ancestry, indicating that gene flow from European wild boars resulted in a near-complete disappearance of Near East ancestry. In addition, we demonstrate that a variant at a locus encoding black coat color likely originated in the Near East and persisted in European pigs. Altogether, our results indicate that while pigs were not independently domesticated in Europe, the vast majority of human-mediated selection over the past 5,000 y focused on the genomic fraction derived from the European wild boars, and not on the fraction that was selected by early Neolithic farmers over the first 2,500 y of the domestication process.

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          Most cited references51

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          Massive migration from the steppe was a source for Indo-European languages in Europe

          We generated genome-wide data from 69 Europeans who lived between 8,000-3,000 years ago by enriching ancient DNA libraries for a target set of almost 400,000 polymorphisms. Enrichment of these positions decreases the sequencing required for genome-wide ancient DNA analysis by a median of around 250-fold, allowing us to study an order of magnitude more individuals than previous studies and to obtain new insights about the past. We show that the populations of Western and Far Eastern Europe followed opposite trajectories between 8,000-5,000 years ago. At the beginning of the Neolithic period in Europe, ∼8,000-7,000 years ago, closely related groups of early farmers appeared in Germany, Hungary and Spain, different from indigenous hunter-gatherers, whereas Russia was inhabited by a distinctive population of hunter-gatherers with high affinity to a ∼24,000-year-old Siberian. By ∼6,000-5,000 years ago, farmers throughout much of Europe had more hunter-gatherer ancestry than their predecessors, but in Russia, the Yamnaya steppe herders of this time were descended not only from the preceding eastern European hunter-gatherers, but also from a population of Near Eastern ancestry. Western and Eastern Europe came into contact ∼4,500 years ago, as the Late Neolithic Corded Ware people from Germany traced ∼75% of their ancestry to the Yamnaya, documenting a massive migration into the heartland of Europe from its eastern periphery. This steppe ancestry persisted in all sampled central Europeans until at least ∼3,000 years ago, and is ubiquitous in present-day Europeans. These results provide support for a steppe origin of at least some of the Indo-European languages of Europe.
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            A genetic atlas of human admixture history.

            Modern genetic data combined with appropriate statistical methods have the potential to contribute substantially to our understanding of human history. We have developed an approach that exploits the genomic structure of admixed populations to date and characterize historical mixture events at fine scales. We used this to produce an atlas of worldwide human admixture history, constructed by using genetic data alone and encompassing over 100 events occurring over the past 4000 years. We identified events whose dates and participants suggest they describe genetic impacts of the Mongol empire, Arab slave trade, Bantu expansion, first millennium CE migrations in Eastern Europe, and European colonialism, as well as unrecorded events, revealing admixture to be an almost universal force shaping human populations.
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              The hidden side of invasions: massive introgression by local genes.

              Despite hundreds of reports involving both plants and animals, the mechanisms underlying introgression remain obscure, even if some form of selection is frequently invoked. Introgression has repeatedly been reported in species that have recently colonized a new habitat, suggesting that demographic processes should be given more attention for understanding the mechanisms of introgression. Here we show by spatially explicit simulations that massive introgression of neutral genes takes place during the invasion of an occupied territory if interbreeding is not severely prevented between the invading and the local species. We also demonstrate that introgression occurs almost exclusively from the local to the invading species, especially for populations located far away from the source of the invasion, and this irrespective of the relative densities of the two species. This pattern is strongest at markers experiencing reduced gene flow, in keeping with the observation that organelle genes are often preferentially introgressed across species boundaries. A survey of the literature shows that a majority of published empirical studies of introgression during range expansions, in animals and in plants, follow the predictions of our model. Our results imply that speciation genes can be identified by comparing genomes of interfertile native and invading species pairs.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                27 August 2019
                12 August 2019
                12 August 2019
                : 116
                : 35
                : 17231-17238
                Affiliations
                [1] aSchool of Biological and Chemical Sciences, Queen Mary University of London , London E1 4NS, United Kingdom;
                [2] bThe Palaeogenomics & Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford , Oxford OX1 3TG, United Kingdom;
                [3] cDepartment of Zoology, University of Oxford , Oxford OX1 3SZ, United Kingdom;
                [4] dPalaeogenetics Group, Institute of Organismic and Molecular Evolution, Johannes Gutenberg-University Mainz , D-55128 Mainz, Germany;
                [5] eDepartment of Natural Sciences, German Archaeological Institute , 14195 Berlin, Germany;
                [6] fBioArCh, Department of Archaeology, University of York , York YO10 5NG, United Kingdom;
                [7] gDepartment of Anthropology, Texas A&M University , College Station, TX 77840;
                [8] hDepartment of Earth Sciences, Natural History Museum, London SW7 5BD, United Kingdom;
                [9] iMolecular Population Genetics, Smurfit Institute of Genetics, Trinity College Dublin , Dublin 2, Ireland;
                [10] jDepartment of Anthropology, University of Michigan , Ann Arbor, MI 48109;
                [11] kDepartment of Materials Science and Engineering, Massachusetts Institute of Technology , Cambridge, MA 02142;
                [12] lDepartment of Archaeology, Durham University , Durham DH1 3LE, United Kingdom;
                [13] mCNRS UMR 7044, Maison interuniversitaire des sciences de l’Homme , F-67083 Strasbourg Cedex, France;
                [14] nDepartment of Genetics, Development and Molecular Biology, School of Biology, Aristotle University of Thessaloniki , 54124 Thessaloniki, Greece;
                [15] oDepartment of Anthropology, University of North Carolina at Chapel Hill , Chapel Hill, NC 27599;
                [16] p“Vasile Pârvan” Institute of Archaeology , Bucharest 010667, Romania;
                [17] qOsteoarchaeological Research Laboratory, Department of Archaeology and Classical Studies, Stockholm University , 106 91 Stockholm, Sweden;
                [18] rLaboratory of Theriology, Zoological Institute of the Russian Academy of Sciences , St. Petersburg 199034, Russia;
                [19] sSchool of History, Classics and Archaeology, University of Edinburgh , Edinburgh EH8 9AG, United Kingdom;
                [20] tThe Italian Academy for Advanced Studies in America, Columbia University , New York, NY 10027;
                [21] uLaboratory for Bioarchaeology, Department of Archaeology, Faculty of Philosophy, University of Belgrade , 11000 Belgrade, Serbia;
                [22] vInstitute of Archaeology, University of Groningen , 9712 ER, Groningen, The Netherlands;
                [23] wLaboratorio de Evolución Humana, Departamento de Historia, Geografía y Comunicación Universidad de Burgos , Burgos, Spain;
                [24] xAnimal Breeding and Genomics Center, Wageningen University and Research , 6708 PB Wageningen, The Netherlands;
                [25] yOD Earth and History of Life, Royal Belgian Institute of Natural Sciences , 1000 Brussels, Belgium;
                [26] zCentro de Arqueologia da Universidade de Lisboa , Faculdade de Letras da Universidade de Lisboa, Alameda da Universidade, 1600-214 Lisboa, Portugal;
                [27] aaDepartment of Biological and Geographical Sciences, University of Huddersfield , Huddersfield HD1 3DH, United Kingdom;
                [28] bbDepartment of Archaeology, Gazi University , Ankara 06500, Turkey;
                [29] ccDepartment of Archaeology, Çanakkale Onsekiz Mart University , Çanakkale 17100, Turkey;
                [30] ddFlanders Heritage Agency , 1000 Brussels, Belgium;
                [31] eeDepartment of Biology, University of Naples Federico II , 80126 Napoli, Italy;
                [32] ffHistory, Archaeology and Museology Department, 1 Decembrie 1918 University , Alba Iulia 510009, Romania;
                [33] ggDepartment of Archaeology and Classical Studies, Stockholm University , SE-106 91 Stockholm, Sweden;
                [34] hhUniversité Côte d’Azur , CNRS, Cultures et Environnement, Préhistoire, Antiquité, Moyen Âge (UMR 7264), 06357 Nice, France;
                [35] iiCNRS , Archéorient (UMR 5133), Maison de l’Orient et de la Méditerranée, 69007 Lyon, France;
                [36] jjDepartment of Evolutionary Studies of Biosystems, Graduate University for Advanced Studies , Hayama, Kanagawa 240-0193, Japan;
                [37] kkNational Natural History Collections, Faculty of Life Science, The Hebrew University of Jerusalem , Jerusalem 91904, Israel;
                [38] llDepartment of Archaeology, Classics and Egyptology, University of Liverpool , Liverpool L69 7WZ, United Kingdom;
                [39] mmUnité Archéozoologie, Archéobotanique, Sociétés Pratiques et Environnements (AASPE), CNRS , Muséum National d’Histoire Naturelle, 75020 Paris, France;
                [40] nnSchool of Natural and Built Environment, Queen’s University Belfast , Belfast BT9 5AG, United Kingdom;
                [41] ooScientific Center of Zoology and Hydroecology, Institute of Zoology , Yerevan 0014, Armenia;
                [42] ppInstitute of Archaeology, Adam Mickiewicz University , 61-712, Poznań, Poland;
                [43] qqThe Hellenic Archaeological Research Foundation , Tivoli House, Cheltenham GL50 2TD, United Kingdom;
                [44] rrDepartment of Archaeology, University of Reading , Reading RG6 6AB, United Kingdom;
                [45] ssLithuanian Institute of History, Vilnius University , LT-01513 Vilnius, Lithuania;
                [46] ttInstitut für Archäologische Wissenschaften, Goethe University of Frankfurt , 60323 Frankfurt, Germany;
                [47] uuInternational Union for Conservation of Nature/Species Survival Commission Wild Pig Specialist Group, 15412 Jakarta, Indonesia;
                [48] vvCenter of Excellence for Environmental Decisions, University of Queensland , St Lucia, QLD 4072, Australia;
                [49] wwDurrell Institute of Conservation and Ecology, School of Anthropology and Conservation, Marlowe Building, University of Kent , Canterbury, Kent CT2 7NR, United Kingdom;
                [50] xxAnthropology Department, Hunter College and Graduate Center, City University of New York , New York, NY 10065;
                [51] yyService de Préhistoire, Université de Liège , 4000 Liège, Belgium;
                [52] zzInstitute of Prehistoric Archaeology, Free University of Berlin , 14195 Berlin, Germany;
                [53] aaaCurt-Engelhorn-Zentrum Archäometrie, 68159 Mannheim, Germany;
                [54] bbbEphorate of Paleoanthropology and Speleology , Greek Ministry of Culture, 106 82 Athens, Greece;
                [55] cccInstitute of Archaeology, University College London , London WC1H 0PY, United Kingdom;
                [56] dddDepartment of Evolutionary Anthropology, University of Vienna , 1090 Vienna, Austria;
                [57] eeeMuseum of Vojvodina , 21101 Novi Sad, Serbia;
                [58] fffLaboratoire Évolution & Diversité Biologique-UMR 5174, Université de Toulouse Midi-Pyrénées , 31062 cedex 9 Toulouse, France;
                [59] gggDepartment of Archaeology, Simon Fraser University , Burnaby, BC V5A 1S6, Canada;
                [60] hhhDivision of Vertebrates, Department of Life Sciences, The Natural History Museum , London SW7 5BD, United Kingdom;
                [61] iiiDipartimento di Scienze storiche e dei Beni Culturali, University of Siena , 53100 Siena, Italy;
                [62] jjjOsteologie, Landesamt für Denkmalpflege im Regierungspräsidium Stuttgart , 73728 Konstanz, Germany;
                [63] kkkFaculty of Science and Technology, Bournemouth University , Fern Barrow, Poole, Dorset BH12 5BB, United Kingdom;
                [64] lllMagdalene College, University of Cambridge , Cambridge CB3 0AG, United Kingdom;
                [65] mmmSezione di Bioarcheologia, Museo delle Civiltà , 00144 Roma, Italy;
                [66] nnnDepartment of Archaeology, Faculty of Philosophy, University of Belgrade , 11000 Belgrade, Serbia;
                [67] oooDepartment of Archaeology and History, Faculty of Humanities and Social Sciences, La Trobe University , Melbourne, MB 167, Australia;
                [68] pppInstitute of Archaeology of the National Academy of Sciences of Ukraine , 02000 Kiev, Ukraine;
                [69] qqqGeneraldirektion Kulturelles Erbe Rheinland-Pfalz, Dir. Landesarchäologie, D–67346 Speyer, Germany;
                [70] rrrNatural History Museum of Denmark, University of Copenhagen , DK-1123 Copenhagen, Denmark;
                [71] sssUniversity Museum, Norwegian University of Science and Technology , 7012 Trondheim, Norway;
                [72] tttIntegrative Prehistory and Archaeological Science, University of Basel , 4055 Basel, Switzerland;
                [73] uuuDepartment of Anthropology, National Museum of Natural History, Smithsonian Institution , Washington, DC 37012;
                [74] vvvArchaeoBioCenter and Department of Veterinary Sciences, Institute of Palaeoanatomy, Domestication and the History of Veterinary Medicine, Ludwig Maximilian University Munich , 80539 Munich, Germany;
                [75] wwwState Collection for Anthropology and Palaeoanatomy, Bavarian Natural History Collections, 80333 Munich, Germany;
                [76] xxxDepartment of Archaeology, School of Geosciences, University of Aberdeen , St. Mary’s, Aberdeen AB24 3FUK, United Kingdom;
                [77] yyyInstitut des Sciences de l’Evolution-Montpellier-UMR 5554-CNRS, IRD, Université de Montpellier , 34090 Montpellier, France;
                [78] zzzResearch Centre in Evolutionary Anthropology and Palaeoecology, School of Natural Sciences and Psychology, Liverpool John Moores University , Liverpool L3 3AF, United Kingdom
                Author notes
                2To whom correspondence may be addressed. Email: laurent.frantz@ 123456qmul.ac.uk or greger.larson@ 123456arch.ox.ac.uk .

                Edited by Dolores R. Piperno, Smithsonian Institution, Washington, DC, and approved June 24, 2019 (received for review February 8, 2019)

                Author contributions: L.A.F.F., L.G.-F., and G.L. designed research; L.A.F.F., J.H., V.E.M., K.G.D., O.L., T.C., A. Evin, and L.G.-F. performed research; L.A.F.F., J.H., A.S., C.G., N.B., M.A., A.L., V.E.M., K.G.D., M.P., K.J.G., P.A., R.-M.A., B.A., A. Bălăşescu, R.B., L.B., G.B., C.B., D.B., A. Boroneant, J. Bulatović, C.Ç., J.-M.C., J.C., M.C., R.C., B.D.C., C.D., V. Dimitrijevic, V. Dumitrașcu, C.J.E., C.M.E., A.E.-Ö., A. Ervynck, D.F., M.G., A.G., L.G., M.A.M.G., D.H., H.H., L.K.H., O.L., J.L., C.M., N.M., A.M., H.M., M.M., R. Matthews, G.M.M., S.M., E.M., T.M., H.-J.M., R. Miller, A.M., J.O., D.O., A.P., M.P.P., R.P., D.R., F.-X.R., M.R., R.S., L.S., W.S., S. Sheikhi, E.S., J.R.S., S. Stoddart, A. Tagliacozzo, N.T., K.T., A. Tresset, C.V., Y.v.d.H., S.V.P., J.-D.V., A.Y., A.Z.-L., A. Triantafyllidis, M.T.P.G., J.S., P.R.-C., M.Z., J.P., T.C., D.G.B., K.D., J. Burger, A. Evin, L.G.-F., and G.L. contributed new reagents/analytic tools; L.A.F.F., A.T.L., V.M.B., L.d.P., and E.K.I.-P. analyzed data; and L.A.F.F., A.T.L., K.J.G., P.R.-C., M.Z., J.P., and G.L. wrote the paper.

                1L.A.F.F., J.H., and A.T.L. contributed equally to this work.

                3Deceased March 20, 2017.

                4Deceased January 17, 2019.

                Author information
                http://orcid.org/0000-0003-2505-1480
                http://orcid.org/0000-0001-7834-5111
                http://orcid.org/0000-0002-5160-5902
                http://orcid.org/0000-0003-1940-2192
                http://orcid.org/0000-0001-8685-3685
                http://orcid.org/0000-0001-5274-8887
                http://orcid.org/0000-0003-4515-1649
                http://orcid.org/0000-0001-6499-8728
                http://orcid.org/0000-0002-4092-0392
                Article
                201901169
                10.1073/pnas.1901169116
                6717267
                31405970
                8df90741-7256-4cea-8b5d-1dec45651742
                Copyright © 2019 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).

                History
                Page count
                Pages: 8
                Categories
                Biological Sciences
                Anthropology

                domestication,evolution,gene flow,neolithic
                domestication, evolution, gene flow, neolithic

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