The evolutionary history of dogs in the Americas

Máire Ní Leathlobhair¹, Angela R Perri^{2

3}, Evan K Irving-Pease⁴, Kelsey E Witt⁵, Anna Linderholm^{4

6}, James Haile^{4

7}, Ophelie Lebrasseur⁴, Carly Ameen⁸, Jeffrey Blick⁹, Adam R Boyko¹⁰, Selina Brace¹¹, Yahaira Nunes Cortes¹², Susan J Crockford¹³, Alison Devault¹⁴, Evangelos A Dimopoulos⁴, Morley Eldridge¹⁵, Jacob Enk¹⁴, Shyam Gopalakrishnan⁷, Kevin Gori¹, Vaughan Grimes¹⁶, Eric Guiry¹⁷, Anders J Hansen^{7

18}, Ardern Hulme-Beaman^{4

8}, John Johnson¹⁹, Andrew Kitchen²⁰, Aleksei K Kasparov²¹, Young-Mi Kwon¹, Pavel A Nikolskiy^{21

22}, Carlos Peraza Lope²³, Aurélie Manin^{24

25}, Terrance Martin²⁶, Michael Meyer²⁷, Kelsey Noack Myers²⁸, Mark Omura²⁹, Jean-Marie Rouillard^{14

30}, Elena Y Pavlova^{21

31}, Paul Sciulli³², Mikkel-Holger S Sinding^{7

18

33}, Andrea Strakova¹, Varvara V Ivanova³⁴, Christopher Widga³⁵, Eske Willerslev⁷, Vladimir V Pitulko²¹, Ian Barnes¹¹, M Thomas P Gilbert^{7

36}, Keith M Dobney^{8

37}, Ripan S Malhi^{38

39}, Elizabeth P Murchison⁴⁰, Greger Larson⁴¹, Laurent A F Frantz^{41

42}

Affiliations

¹ Transmissible Cancer Group, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.
² Department of Archaeology, Durham University, Durham, UK.
³ Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
⁴ The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK.
⁵ School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana-Champaign, IL, USA.
⁶ Department of Anthropology, Texas A&M University, College Station, TX, USA.
⁷ Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
⁸ Department of Archaeology, Classics and Egyptology, University of Liverpool, Liverpool, UK.
⁹ Department of Government and Sociology, Georgia College and State University, Milledgeville, GA, USA.
¹⁰ Department of Biomedical Sciences, Cornell University, Ithaca, NY, USA.
¹¹ Department of Earth Sciences, Natural History Museum, London, UK.
¹² Department of Anthropology, University at Albany-SUNY, Albany, NY, USA.
¹³ Pacific Identifications, Victoria, Canada.
¹⁴ Arbor Biosciences, Ann Arbor, MI, USA.
¹⁵ Millennia Research, Victoria, Canada.
¹⁶ Department of Archaeology, Memorial University, Queen's College, St. John's, Canada.
¹⁷ Department of Anthropology, University of British Columbia, Vancouver, Canada.
¹⁸ The Qimmeq Project, University of Greenland, Nuussuaq, Greenland.
¹⁹ Department of Anthropology, Santa Barbara Museum of Natural History, Santa Barbara, CA, USA.
²⁰ Department of Anthropology, University of Iowa, Iowa City, IA, USA.
²¹ Institute for the History of Material Culture, Russian Academy of Sciences, St. Petersburg, Russia.
²² Geological Institute, Russian Academy of Sciences, Moscow, Russia.
²³ Centro INAH Yucatán, Mérida, Yucatán, México.
²⁴ Department of Archaeology, BioArCh, University of York, York, UK.
²⁵ UMR 7209, Archéozoologie, Archéobotanique, Muséum National d'Histoire Naturelle, Paris, France.
²⁶ Research and Collections Center, Illinois State Museum, Springfield, IL, USA.
²⁷ Touray & Meyer Veterinary Clinic, Serrekunda, Gambia.
²⁸ Glenn A. Black Laboratory of Anthropology, Indiana University Bloomington, Bloomington, IN, USA.
²⁹ Department of Mammalogy, Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA.
³⁰ Department of Chemical Engineering, University of Michigan, Ann Arbor, MI, USA.
³¹ Arctic & Antarctic Research Institute, St. Petersburg, Russia.
³² Department of Anthropology, Ohio State University, Columbus, OH, USA.
³³ Natural History Museum, University of Oslo, Oslo, Norway.
³⁴ VNIIOkeangeologia Research Institute, St. Petersburg, Russia.
³⁵ Center of Excellence in Paleontology, East Tennessee State University, Gray, TN, USA.
³⁶ Norwegian University of Science and Technology, University Museum, Trondheim, Norway.
³⁷ Department of Archaeology, University of Aberdeen, Aberdeen, UK.
³⁸ Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana-Champaign, IL, USA.
³⁹ Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana-Champaign, IL, USA.
⁴⁰ Transmissible Cancer Group, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK. laurent.frantz@qmul.ac.uk greger.larson@arch.ox.ac.uk epm27@cam.ac.uk.
⁴¹ The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK. laurent.frantz@qmul.ac.uk greger.larson@arch.ox.ac.uk epm27@cam.ac.uk.
⁴² School of Biological and Chemical Sciences, Queen Mary University of London, London, UK.

PMID: 29976825
PMCID: PMC7116273
DOI: 10.1126/science.aao4776

The evolutionary history of dogs in the Americas

Máire Ní Leathlobhair et al. Science. 2018.

. 2018 Jul 6;361(6397):81-85.

doi: 10.1126/science.aao4776.

Authors

Affiliations

¹ Transmissible Cancer Group, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK.
² Department of Archaeology, Durham University, Durham, UK.
³ Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
⁴ The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK.
⁵ School of Integrative Biology, University of Illinois at Urbana-Champaign, Urbana-Champaign, IL, USA.
⁶ Department of Anthropology, Texas A&M University, College Station, TX, USA.
⁷ Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.
⁸ Department of Archaeology, Classics and Egyptology, University of Liverpool, Liverpool, UK.
⁹ Department of Government and Sociology, Georgia College and State University, Milledgeville, GA, USA.
¹⁰ Department of Biomedical Sciences, Cornell University, Ithaca, NY, USA.
¹¹ Department of Earth Sciences, Natural History Museum, London, UK.
¹² Department of Anthropology, University at Albany-SUNY, Albany, NY, USA.
¹³ Pacific Identifications, Victoria, Canada.
¹⁴ Arbor Biosciences, Ann Arbor, MI, USA.
¹⁵ Millennia Research, Victoria, Canada.
¹⁶ Department of Archaeology, Memorial University, Queen's College, St. John's, Canada.
¹⁷ Department of Anthropology, University of British Columbia, Vancouver, Canada.
¹⁸ The Qimmeq Project, University of Greenland, Nuussuaq, Greenland.
¹⁹ Department of Anthropology, Santa Barbara Museum of Natural History, Santa Barbara, CA, USA.
²⁰ Department of Anthropology, University of Iowa, Iowa City, IA, USA.
²¹ Institute for the History of Material Culture, Russian Academy of Sciences, St. Petersburg, Russia.
²² Geological Institute, Russian Academy of Sciences, Moscow, Russia.
²³ Centro INAH Yucatán, Mérida, Yucatán, México.
²⁴ Department of Archaeology, BioArCh, University of York, York, UK.
²⁵ UMR 7209, Archéozoologie, Archéobotanique, Muséum National d'Histoire Naturelle, Paris, France.
²⁶ Research and Collections Center, Illinois State Museum, Springfield, IL, USA.
²⁷ Touray & Meyer Veterinary Clinic, Serrekunda, Gambia.
²⁸ Glenn A. Black Laboratory of Anthropology, Indiana University Bloomington, Bloomington, IN, USA.
²⁹ Department of Mammalogy, Museum of Comparative Zoology, Harvard University, Cambridge, MA, USA.
³⁰ Department of Chemical Engineering, University of Michigan, Ann Arbor, MI, USA.
³¹ Arctic & Antarctic Research Institute, St. Petersburg, Russia.
³² Department of Anthropology, Ohio State University, Columbus, OH, USA.
³³ Natural History Museum, University of Oslo, Oslo, Norway.
³⁴ VNIIOkeangeologia Research Institute, St. Petersburg, Russia.
³⁵ Center of Excellence in Paleontology, East Tennessee State University, Gray, TN, USA.
³⁶ Norwegian University of Science and Technology, University Museum, Trondheim, Norway.
³⁷ Department of Archaeology, University of Aberdeen, Aberdeen, UK.
³⁸ Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana-Champaign, IL, USA.
³⁹ Carl R. Woese Institute for Genomic Biology, University of Illinois at Urbana-Champaign, Urbana-Champaign, IL, USA.
⁴⁰ Transmissible Cancer Group, Department of Veterinary Medicine, University of Cambridge, Cambridge, UK. laurent.frantz@qmul.ac.uk greger.larson@arch.ox.ac.uk epm27@cam.ac.uk.
⁴¹ The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK. laurent.frantz@qmul.ac.uk greger.larson@arch.ox.ac.uk epm27@cam.ac.uk.
⁴² School of Biological and Chemical Sciences, Queen Mary University of London, London, UK.

PMID: 29976825
PMCID: PMC7116273
DOI: 10.1126/science.aao4776

Abstract

Dogs were present in the Americas before the arrival of European colonists, but the origin and fate of these precontact dogs are largely unknown. We sequenced 71 mitochondrial and 7 nuclear genomes from ancient North American and Siberian dogs from time frames spanning ~9000 years. Our analysis indicates that American dogs were not derived from North American wolves. Instead, American dogs form a monophyletic lineage that likely originated in Siberia and dispersed into the Americas alongside people. After the arrival of Europeans, native American dogs almost completely disappeared, leaving a minimal genetic legacy in modern dog populations. The closest detectable extant lineage to precontact American dogs is the canine transmissible venereal tumor, a contagious cancer clone derived from an individual dog that lived up to 8000 years ago.

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Conflict of interest statement

Competing interests: A.D., J.E, and J-M.R. are employees of Arbor Biosciences which provided target enrichment kits used in this study. J-M.R. is also a founder of Arbor Biosciences. KD currently holds honorary Professor positions in the Departments of Archaeology at both the University of Aberdeen and Simon Fraser University. A significant portion of the research included in this paper (along with associated NERC funding) was also undertaken whilst KD was a full-time member of faculty at the University of Aberdeen. A.R.B. is founder and CSO of Embark Veterinary.

Figures

**Figure 1. Sample location and ancestry of pre-contact dogs**
a.A map depicting the location and age of the archeological remains analyzed in this study. Each dot represents a single sample, and multiple samples per archeological site are grouped in boxes. Sites mentioned in the text are labelled. b. A tip calibrated Bayesian mitochondrial phylogenetic tree of dogs, within haplogroup A. This analysis was conducted with 71 novel ancient mitogenomes together with 145 publicly available mitogenomes from both modern and ancient canids (3) (Fig. S6). Red branches represent modern dogs. Blue horizontal bars on nodes represent 95% High Density Posterior age. The grey shaded area represents the time frame during which people entered the Americas (–12) c. A neighbor-joining tree built with whole genomes (3). d An admixture graph constructed with *TreeMix* (based on transversions; (3)) depicting the relationship between PCD (including the Port Du Choix [AL3194] and Weyanoke Old Town [AL3223] samples) and other dog and wolf populations. We only used Greenland dogs and Malamute (American Arctic dogs) for this analysis as these are the least admixed with Western Eurasian dogs (3).

**Figure 2. Legacy of pre-contact dogs in modern american dogs**
a. A map showing the locations of dog populations obtained from (9) and their degree of relatedness (D-statistics) with the ~4ky old Port au Choix dog (AL3194; see (3) and Fig. S14). Higher values (in red) represent closer relatedness. b. A map depicting the multiple introductions of dogs into the Americas.

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Comment in

America's lost dogs.
Goodman L, Karlsson EK. Goodman L, et al. Science. 2018 Jul 6;361(6397):27-28. doi: 10.1126/science.aau1306. Epub 2018 Jul 5. Science. 2018. PMID: 29976811 No abstract available.

References

1. Larson G, et al. Rethinking dog domestication by integrating genetics, archeology, and biogeography. Proc Natl Acad Sci U S A. 2012;109:8878–8883. - PMC - PubMed
1. Perri A, et al. New evidence of the earliest domestic dogs in the Americas. Am Antiq. 2018
1. See supplementary materials.
1. Goebel T, Waters MR, O’Rourke DH. The late Pleistocene dispersal of modern humans in the Americas. Science. 2008;319:1497–1502. - PubMed
1. Leonard JA, et al. Ancient DNA evidence for Old World origin of New World dogs. Science. 2002;298:1613–1616. - PubMed

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The evolutionary history of dogs in the Americas

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The evolutionary history of dogs in the Americas

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