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Ancient DNA Suggests Modern Wolves Trace Their Origin to a Late Pleistocene Expansion from Beringia

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Ancient DNA Suggests Modern Wolves Trace Their Origin to a Late Pleistocene Expansion from Beringia Received: 5 October 2018 | Revised: 16 October 2019 | Accepted: 3 December 2019 DOI: 10.1111/mec.15329 FROM THE COVER Ancient DNA suggests modern wolves trace their origin to a Late Pleistocene expansion from Beringia Liisa Loog1,2,3,4 | Olaf Thalmann5 | Mikkel-Holger S. Sinding6,7,8 | Verena J. Schuenemann9,10,11 | Angela Perri12 | Mietje Germonpré13 | Herve Bocherens10,14 | Kelsey E. Witt15 | Jose A. Samaniego Castruita6 | Marcela S. Velasco6 | Inge K. C. Lundstrøm6 | Nathan Wales6,16 | Gontran Sonet17 | Laurent Frantz2 | Hannes Schroeder6 | Jane Budd18 | Elodie-Laure Jimenez13 | Sergey Fedorov19 | Boris Gasparyan20 | Andrew W. Kandel21 | Martina Lázničková-Galetová22,23,24 | Hannes Napierala25 | Hans-Peter Uerpmann9 | Pavel A. Nikolskiy26,27 | Elena Y. Pavlova27,28 | Vladimir V. Pitulko27 | Karl-Heinz Herzig5,29 | Ripan S. Malhi30 | Eske Willerslev2,31,32 | Anders J. Hansen8,31 | Keith Dobney33,34,35 | M. Thomas P. Gilbert6,36 | Johannes Krause9,37 | Greger Larson1 | Anders Eriksson2,38,39 | Andrea Manica2 1Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK 2Department of Zoology, University of Cambridge, Cambridge, UK 3Manchester Institute of Biotechnology, School of Earth and Environmental Sciences, University of Manchester, Manchester, UK 4Department of Genetics, University of Cambridge, Cambridge, UK 5Department of Pediatric Gastroenterology and Metabolic Diseases, Poznan University of Medical Sciences, Poznan, Poland 6EvoGenomics, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark 7Natural History Museum, University of Oslo, Oslo, Norway 8The Qimmeq Project, University of Greenland, Nuussuaq, Greenland 9Institute for Archaeological Sciences, University of Tübingen, Tübingen, Germany 10Senckenberg Centre for Human Evolution and Palaeoenvironment, University of Tübingen, Tübingen, Germany 11Institute of Evolutionary Medicine, University of Zurich, Zurich, Switzerland 12Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany 13OD Earth and History of Life, Royal Belgian Institute of Natural Sciences, Brussels, Belgium 14Department of Geosciences, Palaeobiology, University of Tübingen, Tübingen, Germany 15School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA 16BioArch, Department of Archaeology, University of York, York, UK, USA 17OD Taxonomy and Phylogeny, Royal Belgian Institute of Natural Sciences, Brussels, Belgium 18Breeding Centre for Endangered Arabian Wildlife, Sharjah, United Arab Emirates 19Mammoth Museum, Institute of Applied Ecology of the North of the North-Eastern Federal University, Yakutsk, Russia 20Institute of Archaeology and Ethnography, National Academy of Sciences of the Republic of Armenia, Yerevan, Republic of Armenia 21Heidelberg Academy of Sciences and Humanities: The Role of Culture in Early Expansions of Humans, Tübingen, Germany 22Department of Anthropology, University of West Bohemia, Pilzen, Czech Republic 23Moravian museum, Brno, Czech Republic Thalmann, Sinding, and Schuenemann contributed equally to this work. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Molecular Ecology published by John Wiley & Sons Ltd Molecular Ecology. 2019;00:1–15. wileyonlinelibrary.com/journal/mec | 1 2 | LOOG ET AL. 24Hrdlička Museum of Man, Faculty of Science, Charles University, Praha, Czech Republic 25Institute of Palaeoanatomy, Domestication Research and History of Veterinary Medicine, Ludwig-Maximilians-University Munich, Munich, Germany 26Geological Institute, Russian Academy of Sciences, Moscow, Russia 27Institute for Material Culture History, Russian Academy of Sciences, St Petersburg, Russia 28Arctic and Antarctic Research Institute, St Petersburg, Russia 29Institute of Biomedicine and Biocenter of Oulu, Medical Research Center and University Hospital, University of Oulu, Oulu, Finland 30Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana, IL, USA 31Centre for GeoGenetics Globe Institute, University of Copenhagen, Copenhagen, Denmark 32Wellcome Trust Sanger Institute, Cambridge, UK 33Department of Archaeology, Classics and Egyptology, University of Liverpool, Liverpool, UK 34Department of Archaeology, University of Aberdeen, Aberdeen, UK 35Department of Archaeology, Simon Fraser University, Burnaby, BC, Canada 36Norwegian University of Science and Technology, University Museum, Trondheim, Norway 37Max Planck Institute for the Science of Human History, Jena, Germany 38Department of Medical & Molecular Genetics, King's College London, Guys Hospital, London, UK 39cGEM, Institute of Genomics, University of Tartu, Tartu, Estonia Correspondence Liisa Loog, Department of Genetics, Markova,Abstract 2016), and both the palaeontological and archaeological records attest to the continu- University of Cambridge, Cambridge, UK. ousGrey presence wolves of (greyCanis wolves lupus across) are onethe Northernof the few Hemisphere large terrestrial for at least carnivores the last 300,000 that have years Email: [email protected] (Sotnikovamaintained & Rook, a wide 2010) geographical (reviewed in Appendix distribution S1). Thisacross geographical the Northern and temporal Hemisphere continuity Greger Larson, Research Laboratory for across the Northern Hemisphere contrasts with analyses of complete modern genomes, which throughout the Pleistocene and Holocene. Recent genetic studies have suggested Archaeology and History of Art, University have suggested that all contemporary wolves and dogs descend from a common ancestral popula- of Oxford, Oxford, UK. that, despite this continuous presence, major demographic changes occurred in wolf tion that existed as recently as 20,000 years ago (Fan et al., 2016; Freedman et al., 2014; Skoglund, Email: [email protected] Ersmark,populations Palkopoulou, between & Dalén,the Late 2015). Pleistocene and early Holocene, and that extant wolves Anders Eriksson, cGEM, Institute of traceThese their analyses ancestry point to to a bottlenecksingle Late followed Pleistocene by a rapid population. radiation Bothfrom anthe ancestral geographical popula - Genomics, University of Tartu, Tartu, Estonia. tionorigin around of this or just ancestral after the population LGM. The geographicaland how it originbecame and widespread dynamics of remainthis radiation unknown. remain Email: [email protected] unknown.Here, we Resolving used a spatiallythese demographic and temporally changes explicit is necessary modelling for frameworkunderstanding to theanalyse ecologi a - cal circumstances that allowed wolves to survive the Late Pleistocene megafaunal extinctions. Andrea Manica, Department of Zoology, data set of 90 modern and 45 ancient mitochondrial wolf genomes from across the University of Cambridge, Cambridge, UK. Furthermore, because dogs were domesticated from Late Pleistocene grey wolves (Larson et al., Northern Hemisphere, spanning the last 50,000 years. Our results suggest that con- Email: [email protected] 2012), a detailed insight into wolf demography during this time period would provide an essential contexttemporary for reconstructing wolf populations the history trace of their dog ancestrydomestication. to an expansion from Beringia at the Funding information Russian Science Foundation, Grant/Award endReconstructing of the Last Glacial past demographic Maximum, andevents that solely this processfrom modern was most genomes likely is driven challenging by Late be - Number: N16-18-10265 RNF; Grantová causePleistocene multiple demographicecological fluctuations histories can that lead occurredto similar geneticacross patternsthe Northern in present-day Hemisphere. samples Agentura České Republiky, Grant/Award (Groucutt et al., 2015). Analyses that incorporate ancient DNA sequences can eliminate some of Number: GAČR15-06446S; Polish National This study provides direct ancient genetic evidence that long-range migration has Science Center, Grant/Award Number: theseplayed alternative an important histories role by quantifyingin the population changes historyin population of a large genetic carnivore, differences and through provides time. 2015/19/P/NZ7/03971; Lundbeckfonden, While nuclear markers provide greater power relative to mitochondrial DNA (mtDNA), the latter insight into how wolves survived the wave of megafaunal extinctions at the end of Grant/Award Number: R52-5062; is more easily retrievable and better preserved in ancient samples due to its higher copy number Natural Environment Research Council, the last glaciation. Moreover, because Late Pleistocene grey wolves were the likely compared to nuclear DNA, thus allowing for the generation of data sets with greater geographi- Grant/Award Number: NE/K003259/1 and NE/K005243/1; H2020 European calsource and temporal from which coverage. all modern In particular, dogs analysing trace their samples origins, dated the to demographic before, during historyand after de the- Research Council, Grant/Award Number: demographicscribed in this events study of hasinterest fundamental greatly increases implications the power for understandingto infer past demographic the geographical histories. 339941-ADAPT, 647787-LocalAdaptation, Furthermore, the nuclear mutation rate in canids is poorly understood, leading to wide date ranges 681396-Extinction Genomics and ERC- origin of the dog. 2013-StG
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