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Ancient DNA, Pig Domestication, and the Spread of the Neolithic Into Europe

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Ancient DNA, Pig Domestication, and the Spread of the Neolithic Into Europe Ancient DNA, pig domestication, and the spread of the Neolithic into Europe Greger Larsona,b,c, Umberto Albarellad, Keith Dobneyb,e, Peter Rowley-Conwyb,Jo¨ rg Schiblerf, Anne Tressetg, Jean-Denis Vigneg, Ceiridwen J. Edwardsh, Angela Schlumbaumf, Alexandru Dinui, Adrian Baˇlaˇ çsescuj, Gaynor Dolmank, Antonio Tagliacozzol, Ninna Manaseryanm, Preston Miraclen, Louise Van Wijngaarden-Bakkero, Marco Massetip, Daniel G. Bradleyh, and Alan Cooperk aDepartment of Zoology, Henry Wellcome Ancient Biomolecules Centre, South Parks Road, Oxford OX1 3PS, United Kingdom; bDepartment of Archaeology, Durham University, South Road, Durham DH1 3L, United Kingdom; dDepartment of Archaeology, University of Sheffield, Northgate House, West Street, Sheffield S1 4ET, United Kingdom; fInstitute for Prehistory and Archaeological Science, Basel University, Spalenring 145, CH-4055 Basel, Switzerland; gDepartment of Ecology and Biodiversity Management, Centre National de la Recherche Scientifique, Muse´um national d’Histoire naturelle, Unite Mixte de Recherche 5197, Baˆtiment 56, 57 rue Cuvier, F-75231 Paris Cedex 05, France; hMolecular Population Genetics, Smurfit Institute, Trinity College, Dublin 2, Ireland; iDepartment of Anthropology, University of Wisconsin, 1180 Observatory Drive, 5240 Social Science Building, Madison, WI 53706; jNational History Museum of Romania, National Center of Pluridisciplinary Research, 12 Calea Victoriei, 30026 Bucharest, Romania; kAustralian Centre for Ancient DNA, University of Adelaide, South Australia 5005, Australia; lSoprintendenza Speciale al Museo Nazionale Preistorico Etnografico L. Pigorini, Sezione di Paleontologia del Quaternario e Archeozoologia, Piazzale G. Marconi 14, 00144 Rome, Italy; mInstitute of Zoology, National Academy of Sciences of Armenia, 7, Sevag str, Yerevan 375014, Armenia; nDepartment of Archaeology, University of Cambridge, Downing Street, Cambridge CB2 3DZ, United Kingdom; oAmsterdam Archaeological Center, University of Amsterdam, Turfdraagsterpad 9, 1012 XT, Amsterdam, The Netherlands; and pDipartimento di Biologia Animale e Genetica ‘‘Leo Pardi’’ dell’Universita`di Firenze, Laboratori di Antropologia, 50121 Firenze, Italy Edited by Ofer Bar-Yosef, Harvard University, Cambridge, MA, and approved July 27, 2007 (received for review April 13, 2007) The Neolithic Revolution began 11,000 years ago in the Near East and Parallel debates also exist with respect to the domestic animals preceded a westward migration into Europe of distinctive cultural associated with the Neolithic revolution, although some cases are groups and their agricultural economies, including domesticated easier to interpret than others. For example, because neither wild animals and plants. Despite decades of research, no consensus has sheep (Ovis orientalis) nor wild goats (Capra aegagrus) were natu- emerged about the extent of admixture between the indigenous and rally distributed across Europe during the Holocene (11–13), the exotic populations or the degree to which the appearance of specific recovery of their remains from European Neolithic archeological components of the ‘‘Neolithic cultural package’’ in Europe reflects sites directly implies their introduction from the Near East (14). truly independent development. Here, through the use of mitochon- The wild ancestors of domestic cows (Bos primigenius), dogs drial DNA from 323 modern and 221 ancient pig specimens sampled (Canis lupus), and pigs (Sus scrofa), however, were widely distrib- across western Eurasia, we demonstrate that domestic pigs of Near uted throughout Europe during the early and mid Holocene, Eastern ancestry were definitely introduced into Europe during the leaving open the possibility of their indigenous domestication Neolithic (potentially along two separate routes), reaching the Paris within Europe. Additionally, the genetic legacy of modern domestic Basin by at least the early 4th millennium B.C. Local European wild animal stocks may have been further complicated by the inter- boar were also domesticated by this time, possibly as a direct con- breeding of independently domesticated European and Near East- sequence of the introduction of Near Eastern domestic pigs. Once ern lineages, just as humans from Near Eastern Neolithic and domesticated, European pigs rapidly replaced the introduced domes- European Mesolithic populations may have done. Deciphering tic pigs of Near Eastern origin throughout Europe. Domestic pigs whether these interactions occurred and what their ramifications formed a key component of the Neolithic Revolution, and this de- may have been, however, has proven as difficult to unravel for tailed genetic record of their origins reveals a complex set of inter- domestic animals as it has for humans. Genetic data from modern actions and processes during the spread of early farmers into Europe. and ancient European cattle, for example, have revealed that although cattle domesticated in the Near East were subsequently European colonization ͉ mtDNA ͉ phylogeography introduced into Europe (14, 15), modern European cattle also possess genes derived from wild aurochsen indigenous to Europe. he transition from hunting to husbandry and the spread of Although this phenomenon has been shown to be the result of Teconomic and cultural elements associated with Neolithic farm- hybridization between European aurochsen and introduced Near ing across Europe between the 7th and 4th millenniums B.C. remain poorly understood despite decades of research. The ques- Author contributions: G.L., U.A., K.D., and P.R.-C. designed research; G.L., U.A., K.D., P.R.-C., tion of how the Neolithic ‘‘package’’ first arrived in Europe has J.S., A. Tresset, J.-D.V., C.J.E., A.S., A.D., A.B., G.D., A. Tagliacozzo, N.M., P.M., L.V.W.-B., focused on three primary hypotheses that assert that the European M.M., and A.C. performed research; G.L., U.A., K.D., P.R.-C., J.S., A. Tresset, J.-D.V., C.J.E., Neolithic resulted from (i) the migration of immigrant farmers from A.S., A.D., A.B., G.D., A. Tagliacozzo, N.M., P.M., L.V.W.-B., M.M., and A.C. analyzed data; and G.L., U.A., K.D., P.R.-C., J.S., A. Tresset, J.-D.V., C.J.E., A.S., A.D., A.B., G.D., D.G.B., and the Near East [demic diffusion (1–3)], (ii) the transmission of ideas A.C. wrote the paper. through established trade and exchange networks (cultural diffu- The authors declare no conflict of interest. sion), or (iii) the independent development of agriculture (including This article is a PNAS Direct Submission. the domestication of some animals such as pigs and cattle) by indigenous European Mesolithic cultures (4, 5), although it has Freely available online through the PNAS open access option. been pointed out that these explanations are not mutually exclusive Abbreviation: LBK, Linearbandkeramik. (6). A separate but related debate has focused on the degree and Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. DQ872931–DQ873203). nature of the interaction between proposed incoming Near Eastern cTo whom correspondence may be sent at the present address: Department of Medical populations and indigenous cultures. Linguistic evidence (7) and Biochemistry and Microbiology, Uppsala Biomedical Center, Box 597, S-751 24 Uppsala, modern human genetic evidence (8) have advocated admixture Sweden. E-mail: [email protected]. between indigenous and incoming cultures, but the issue of whether eTo whom correspondence may be addressed. E-mail: [email protected]. Near Eastern (9) or indigenous European populations (10) have This article contains supporting information online at www.pnas.org/cgi/content/full/ played the more significant role in the genesis of the genomes of 0703411104/DC1. modern Europeans remains contentious. © 2007 by The National Academy of Sciences of the USA 15276–15281 ͉ PNAS ͉ September 25, 2007 ͉ vol. 104 ͉ no. 39 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0703411104 Downloaded by guest on September 29, 2021 Eastern domestics (16), in some cases it has been argued that native Crimea (Fig. 1C) indicates that the distribution of Near Eastern European wild cattle were also independently domesticated (17), a haplotypes probably extended to the north shore of the Black Sea. conclusion that remains contentious (18). Given the apparent long-term integrity of the boundary, it follows Zooarcheological research at sites in eastern Turkey [Hallam that samples found on either side that possess haplotypes not C¸emi (19), C¸ayo¨nu¨ Tepesi (20), and Neval C¸ori (21)] and on matching those of local wild boar most likely represent domestic Cyprus (22) reveals an intensification of the relationship be- pigs (derived from exotic wild boar lineages) that have been tween humans and pigs during the second half of the 9th introduced by humans. millennium B.C. Once domesticated, pigs formed a key compo- The data clearly show that pigs with Near Eastern haplotypes nent of the Neolithic package, as evidenced by their presence in crossed this boundary during the Neolithic and began to appear in numerous Near Eastern and European Neolithic contexts, al- European contexts. Eleven pig specimens, identified as domestic, though, like cows, their endemic or exotic status in European from four Neolithic Romanian sites dating to 5500 B.C. (Fig. 1D) Neolithic contexts remains unresolved (23). possess an 80-bp sequence (the Near Eastern Y1 haplotype) A previous genetic study (24) of modern wild boar and domestic identical to that found in a single recent modern boar from Turkey
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