Taming the late Quaternary phylogeography of the Eurasiatic wild ass through ancient and modern DNA E. Andrew Bennett, Sophie Champlot, Joris Peters, Benjamin S. Arbuckle, Silvia Guimaraes, Melanie Pruvost, Shirli Bar-David, Simon J. M. Davis, Mathieu Gautier, Petra Kaczensky, et al. To cite this version: E. Andrew Bennett, Sophie Champlot, Joris Peters, Benjamin S. Arbuckle, Silvia Guimaraes, et al.. Taming the late Quaternary phylogeography of the Eurasiatic wild ass through ancient and modern DNA. PLoS ONE, Public Library of Science, 2017, 12 (4), 10.1371/journal.pone.0174216. hal- 01608862 HAL Id: hal-01608862 https://hal.archives-ouvertes.fr/hal-01608862 Submitted on 26 May 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License RESEARCH ARTICLE Taming the late Quaternary phylogeography of the Eurasiatic wild ass through ancient and modern DNA E. Andrew Bennett1☯, Sophie Champlot1☯, Joris Peters2,3, Benjamin S. Arbuckle4, Silvia Guimaraes1, MeÂlanie Pruvost2¤a, Shirli Bar-David5³, Simon J. M. Davis6³, Mathieu Gautier7³, Petra Kaczensky8³, Ralph Kuehn9³, Marjan Mashkour10³, Arturo Morales-Muñiz11³, Erich Pucher12³, Jean-FrancËois Tournepiche13³, Hans- Peter Uerpmann14³, Adrian Bălăşescu15³, Mietje GermonpreÂ16³, Can Y. GuÈndem14¤b³, a1111111111 Mahmoud-Reza Hemami17³, Pierre-Elie MoulleÂ18³, Aliye OÈ tzan19³, Margarete Uerpmann14³, a1111111111 Chris Walzer8³, Thierry Grange1³*, Eva-Maria Geigl1³* a1111111111 1 Institut Jacques Monod, UMR7592, CNRS-Universite Paris Diderot, Paris, France, 2 Institute of a1111111111 Palaeoanatomy, Domestication Research and the History of Veterinary Medicine, Ludwig-Maximilian a1111111111 University, Munich, Germany, 3 SNSB, Bavarian State Collection of Anthropology and Palaeoanatomy, MuÈnchen, Germany, 4 Department of Anthropology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, United States of America, 5 Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus, Midreshet Ben-Gurion, Israel, 6 LaboratoÂrio de Arqueociências, (DGPC), Ajuda, Lisbon, Portugal, 7 Centre de Biologie pour la Gestion des Populations CBGP, Montferrier-sur-Lez, France, 8 Research Institute of Wildlife Ecology, OPEN ACCESS University of Veterinary Medicine, Vienna, Austria, 9 Technische UniversitaÈt MuÈnchen, AG Molekulare Citation: Bennett EA, Champlot S, Peters J, Zoologie/Lehrstuhl fuÈr Zoologie, Freising, Germany, 10 CNRS and MuseÂum national d'Histoire naturelle, Arbuckle BS, Guimaraes S, Pruvost M, et al. (2017) UMR 7209, ArcheÂozoologie, archeÂobotanique: socieÂteÂs, pratiques et environnements, DeÂpartement Ecologie et Gestion de la BiodiversiteÂ, Paris, France, 11 Laboratory of Archaeozoology, Dept. Biologia, Universidad Taming the late Quaternary phylogeography of the Autonoma de Madrid, Madrid, Spain, 12 Naturhistorisches Museum, Vienna, Austria, 13 MuseÂe Eurasiatic wild ass through ancient and modern d'Angoulême, Angoulême, France, 14 Eberhard-Karls-UniversitaÈt TuÈbingen, Institut fuÈr Ur- und DNA. PLoS ONE 12(4): e0174216. https://doi.org/ FruÈhgeschichte und ArchaÈologie des Mittelalters, Abteilung AÈ ltere Urgeschichte und QuartaÈroÈkologie, 10.1371/journal.pone.0174216 Zentrum fuÈr Naturwissenschaftliche ArchaÈologie, TuÈbingen, Germany, 15 National History Museum of Romania, National Centre of Pluridisciplinary Research, Bucure ti, Romania, 16 Royal Belgian Institute of Editor: Axel Janke, Senckenberg am Meer ş Natural Sciences, Earth and History of Life, Brussels, Belgium, 17 Department of Natural Resources, Isfahan Deutsches Zentrum fur Marine University of Technology, Isfahan, Iran, 18 MuseÂe de PreÂhistoire ReÂgionale, Menton, France, 19 Ankara Biodiversitatsforschung, GERMANY UÈ niversitesi Dil ve Tarih-Coğrafya FakuÈltesi, Ankara, Turkey Received: December 5, 2016 ☯ These authors contributed equally to this work. Accepted: March 6, 2017 ¤a Current address: Institut Jacques Monod CNRS-Universite Paris Diderot, Paris, France ¤b Current address: Fen Edebiyat FakuÈltesi, Batman UÈ niversitesi, Batman, Turkey Published: April 19, 2017 ³ SBD, SJMD, MG, PK, RK, MM, AMM, EP, JFT and HPU also contributed equally to this work. AB, MG, CYG, MRH, PEM, AO, MU and CW also contributed equally to this work. TG and EMG are co-last authors on Copyright: © 2017 Bennett et al. This is an open this work. access article distributed under the terms of the * [email protected] (EMG); [email protected] (TG) Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Abstract Data Availability Statement: All relevant data are Taxonomic over-splitting of extinct or endangered taxa, due to an incomplete knowledge of within the manuscript, supporting information files, and hosted at the NCBI GenBank repository with both skeletal morphological variability and the geographical ranges of past populations, con- the following accession numbers: KY749126- tinues to confuse the link between isolated extant populations and their ancestors. This is KY749246. particularly problematic with the genus Equus. To more reliably determine the evolution and Funding: The Centre National de la Recherche phylogeographic history of the endangered Asiatic wild ass, we studied the genetic diversity Scientifique CNRS, France, provided the financial and inter-relationships of both extinct and extant populations over the last 100,000 years, support for the project to the Epigenome and Paleogenome group of the Jacques Monod including samples throughout its previous range from Western Europe to Southwest and Institute. University Paris Diderot financed the East Asia. Using 229 bp of the mitochondrial hypervariable region, an approach which PLOS ONE | https://doi.org/10.1371/journal.pone.0174216 April 19, 2017 1 / 28 Eurasiatic wild asses through time and space infrastructure including the high containment allowed the inclusion of information from extremely poorly preserved ancient samples, we laboratory of the Jacques Monod Institute. The classify all non-African wild asses into eleven clades that show a clear phylogeographic Labex "Whom am I" supported E. Andrew Bennett. The French ministry of research supported Sophie structure revealing their phylogenetic history. This study places the extinct European wild th Champlot during her PhD research. The project ass, E. hydruntinus, the phylogeny of which has been debated since the end of the 19 cen- BCS-1311551 "The Origins of Equid Domestication" tury, into its phylogenetic context within the Asiatic wild asses and reveals recent mitochon- of the National Science Foundation NSF granted to drial introgression between populations currently regarded as separate species. The Benjamin S. Arbuckle supported Silvia Guimaraes and contributed to the project. The project DFG-PE phylogeographic organization of clades resulting from these efforts can be used not only to 424/9-1,2 "Ungulate domestication and early improve future taxonomic determination of a poorly characterized group of equids, but also animal husbandry in the Upper Euphratess basin" to identify historic ranges, interbreeding events between various populations, and the impact funded by the Deutsche Forschungsgemeinschaft of ancient climatic changes. In addition, appropriately placing extant relict populations into a to Joris Peters supported MeÂlanie Pruvost. broader phylogeographic and genetic context can better inform ongoing conservation strate- Competing interests: The authors have declared gies for this highly-endangered species. that no competing interests exist. Ethics statement No animals were used in the present study. Samples used in this study and their archeological contexts are described in the Supporting Information and listed in Table A in S1 File. Briefly, we analyzed 189 archaeological bone and teeth specimens that had been assigned osteologically to E. hemionus sp., E. hydruntinus or E. kiang and were dated between 3,500 and 100,000 years ago. These samples originated from 49 archaeological sites in ten European and six southwest Asian countries (Fig 1A and Table A in S1 File). In addition, we analyzed 11 historical museum specimens (between 60 and 180 years old) of onagers, hemippi, khurs and kiangs and 53 pres- ent-day samples, 94% of which originated from wild individuals, coming from the Gobi Desert and protected nature reserves in Iran and Israel. The samples from the Negev desert in Israel came from the Israel Nature and Park Authority (INPA) breeding core and had been collected there between 1989 and 1991 as part of the INPA management activities toward reintroduction (e.g., medical treatment, translocations between enclosures): http://www.parks.org.il/sites/ English/parksandreserves/haibaryotvata/Pages/default.aspx. Introduction The Asiatic wild ass (Equus hemionus), once widely distributed over a vast geographical area, is witnessing