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Phylogeny and Ancient DNA of Sus Provides Insights Into Neolithic Expansion in Island Southeast Asia and Oceania

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Phylogeny and Ancient DNA of Sus Provides Insights Into Neolithic Expansion in Island Southeast Asia and Oceania Phylogeny and ancient DNA of Sus provides insights into neolithic expansion in Island Southeast Asia and Oceania Greger Larsona,b,z, Thomas Cucchic,d, Masakatsu Fujitac, Elizabeth Matisoo-Smithe, Judith Robinse, Atholl Andersonf, Barry Rolettg, Matthew Spriggsh, Gaynor Dolmani, Tae-Hun Kimj, Nguyen Thi Dieu Thuyk, Ettore Randil, Moira Dohertye, Rokus Awe Duem, Robert Bolltg, Tony Djubiantonom, Bion Griffing, Michiko Intohn, Emile Keanec, Patrick Kircho, Kuang-Ti Lip, Michael Morwoodq, Lolita M. Pedrin˜ ar, Philip J. Pipers, Ryan J. Rabettt, Peter Shooteru, Gert Van den Berghv, Eric Westw, Stephen Wicklerx, Jing Yuany, Alan Cooperi, and Keith Dobneyb,c aDepartment of Medical Biochemistry and Microbiology, Uppsala University Biomedical Center, Box 597, 751 24 Uppsala, Sweden; cDepartment of Archaeology, University of Durham, South Road, Durham DH1 3L, United Kingdom; cDepartment of Anthropology and Allan Wilson Centre for Molecular Ecology and Evolution, University of Auckland, P.O. Box 92019, Auckland, New Zealand; gDepartment of Anthropology, University of Hawaii, 2424 Maile Way, Honolulu, HI 96822; fDepartment of Archaeology and Natural History, Research School of Pacific and Asian Studies, and hSchool of Archaeology and Anthropology, Faculty of Arts, The Australian National University, Canberra ACT 0200, Australia; iAustralian Centre for Ancient DNA, Earth, and Environmental Sciences, University of Adelaide, South Australia 5005, Australia; jAnimal Genomics Laboratory, Animal Genomics and Bioinformatics Division, National Livestock Research Institute Rural Development Administration, 564 Omockchun-Dong, Gwonseon-Gu, Suwon 441-706, Korea; kInstitute of Biotechnology Vietnamese Academy of Science and Technology, 18 Hoang Quoc Viet Road, Cau Giay, Ha Noi, Vietnam; lLaboratorio di Genetica, Istituto Nazionale per la Fauna Selvatica, Via Ca`Fornacetta, 9, 40064 Ozzano Emilia Bologna, Italy; mIndonesian Centre for Archaeology, Jl. Raya Condet Pejaten 4, Jakarta 12001, Indonesia; nDepartment of Social Research, National Museum of Ethnology, Osaka 565-8511, Japan; oDepartment of Anthropology, University of California, 232 Kroeber Hall, Berkeley, CA 94720; pInstitute of History and Philology, Academia Sinica, Nankang, Taipei 11529, Taiwan; qDepartment of Archaeology and Palaeoanthropology, School of Human and Environmental Studies, University of New England, Armidale, New South Wales 2351, Australia; rBinirayan Hills, San Jose, Antique, Panay, Philippines; sCentre for Palaeoecology and Evolution, Department of Archaeology, University of York, The King’s Manor, York YO1 7EP, United Kingdom; tThe McDonald Institute for Archaeological Research, University of Cambridge, Downing Street, Cambridge CB2 3ER, United Kingdom; vRoyal Netherlands Institute for Sea Research, NL-1790 AB Den Burg, Texel, The Netherlands; wNaval Facilities Engineering Command Pacific, 258 Makalapa Drive, Pearl Harbor, HI 96860; xDepartment of Archaeology, Tromsø University Museum, N-9037 Tromsø, Norway; yResearch Centre for Archaeological Science, Institute of Archaeology, Chinese Academy of Social Sciences, Beijing 100710, China; u107 Dunbar Street, Mount Gravatt East, Brisbane Q4122, Australia; dDe´partement Ecologie et Gestion de la Biodiversite´, Unite´Mixte de Recherche 5197, Muse´um National d’Histoire Naturelle, 55 Rue Buffon, 75231 Paris Cedex 5, France; and zHenry Wellcome Ancient Biomolecules Centre, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, United Kingdom Edited by Barbara A. Schaal, Washington University, St. Louis, MO, and approved February 2, 2007 (received for review September 5, 2006) Human settlement of Oceania marked the culmination of a global has the extent to which these various components were dispersed colonization process that began when humans first left Africa at as a single unit (7). For example, models of the origins of Lapita least 90,000 years ago. The precise origins and dispersal routes of (the immediate ancestors of the Polynesians and many other the Austronesian peoples and the associated Lapita culture remain Oceanic cultures) that focus on the entire Lapita cultural and contentious, and numerous disparate models of dispersal (based ecological package moving from Taiwan to the Pacific with little primarily on linguistic, genetic, and archeological data) have been interaction (e.g., the ‘‘Express Train’’ or ‘‘Speedboat out of proposed. Here, through the use of mtDNA from 781 modern and Taiwan’’) are contrasted by others that identify broader regions ancient Sus specimens, we provide evidence for an early human- and possibly multiple origins of the various cultural components. mediated translocation of the Sulawesi warty pig (Sus celebensis) Biological data can contribute to this debate through analyses to Flores and Timor and two later separate human-mediated of genetic variation in the domestic and commensal animals that dispersals of domestic pig (Sus scrofa) through Island Southeast were intimately linked with Neolithic cultures and were signif- Asia into Oceania. Of the later dispersal routes, one is unequivo- icant components of human dispersal and exchange networks. cally associated with the Neolithic (Lapita) and later Polynesian Pigs, chickens, dogs, and rats were introduced to the various migrations and links modern and archeological Javan, Sumatran, islands of Near and Remote Oceania by early human settlers, Wallacean, and Oceanic pigs with mainland Southeast Asian S. and studies of Pacific rats (10) and pigs (11, 12) have demon- scrofa. Archeological and genetic evidence shows these pigs were strated their potential as proxies for reconstructing patterns of certainly introduced to islands east of the Wallace Line, including New Guinea, and that so-called ‘‘wild’’ pigs within this region are most likely feral descendants of domestic pigs introduced by early Author contributions: K.D. designed research; G.L., T.C., M.F., E.M.-S., J.R., G.D., T.-H.K., agriculturalists. The other later pig dispersal links mainland East N.T.D.T., E.R., A.C., and K.D. performed research; A.A., B.R., M.S., M.D., R.A.D., R.B., T.D., Asian pigs to western Micronesia, Taiwan, and the Philippines. B.G., M.I., E.K., P.K., K.-T.L., M.M., L.M.P., P.J.P., R.J.R., P.S., G.V.d.B., E.W., S.W., and J.Y. contributed new reagents/analytic tools; G.L., T.C., M.F., E.M.-S., J.R., T.-H.K., N.T.D.T., E.R., These results provide important data with which to test current A.C., and K.D. analyzed data; and G.L., T.C., E.M.-S., A.A., B.R., M.S., M.D., R.A.D., R.B., T.D., models for human dispersal in the region. B.G., M.I., E.K., P.K., K.-T.L., M.M., L.M.P., P.J.P., R.J.R., P.S., G.V.d.B., E.W., S.W., J.Y., A.C., and K.D. wrote the paper. domestication ͉ mtDNA ͉ Pacific colonization ͉ phylogeography The authors declare no conflict of interest. This article is a PNAS direct submission. he peopling of Oceania was one of the most extensive human Abbreviations: ISEA, Island Southeast Asia; HWABC, Henry Wellcome Ancient Biomolecules Tdispersals of the Holocene (1). Uncertainties remain, how- Centre. Data deposition: The sequences reported in this paper have been deposited in the GenBank ever, regarding the geographic origins of modern populations in database (accession nos. DQ779287–DQ779542, DQ779544–DQ779551, and DQ841948– Melanesia, Micronesia, and Polynesia and the origins of their DQ841949). ancestral cultures. A variety of scenarios have been inferred from bTo whom correspondence may be addressed. E-mail: [email protected] or associated material culture, language, and human genetic sig- [email protected]. natures to explain the movement of Neolithic cultures into Near This article contains supporting information online at www.pnas.org/cgi/content/full/ and Remote Oceania (2–9). The degree to which these cultural 0607753104/DC1. and biological elements reflect dispersal has been questioned, as © 2007 by The National Academy of Sciences of the USA 4834–4839 ͉ PNAS ͉ March 20, 2007 ͉ vol. 104 ͉ no. 12 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0607753104 Downloaded by guest on September 25, 2021 Fig. 1. Bayesian (Monte Carlo–Markov chain) consensus tree of 249 Sus mtDNA control region haplotypes rooted by a common warthog (Phacochoerus aethiopicus). Gray (basal) and green (derived) clusters on the tree correspond to general regions on the map where the majority of pigs possess haplotypes within that cluster. The yellow clade represents the Pacific Clade. Yellow stars represent islands on which at least one specimen possessing Pacific Clade haplotypes was identified. The yellow star in Southeast Asia represents the two mainland Asian wild boar samples in Vietnam that possessed this haplotype. Regions on the map are: Mal, peninsular Malaysia; Bor, Borneo; Sum, Sumatra; Jav, Java; Sul, Sulawesi; F, Flores; T, Timor (both in the Lesser Sundas); Mol, Moluccas Islands; PI, Philippines; Tai, Taiwan; NG, New Guinea. The dashed red line labeled WL represents the Wallace Line. The black dashed arrow leading to the more derived portion of the tree illustrates the natural movement of wild Sus out of ISEA and into mainland Asia. See SI Fig. 4 for a more detailed version of the tree. human dispersal into Oceania. A previous genetic study of pigs mined for three archeological pig samples, and an additional 23 (11) revealed a unique Pacific Clade, which included animals ancient samples were characterized with three diagnostic from Halmahera (in the Moluccas), New Guinea, and several Ϸ120-bp fragments by using appropriate ancient DNA methods Pacific
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