Dire wolves were the last of an ancient New World canid lineage – Nature.com

D

Abstract

Dire wolves are considered to be one of the most common and widespread large carnivores in Pleistocene America1, yet relatively little is known about their evolution or extinction. Here, to reconstruct the evolutionary history of dire wolves, we sequenced five genomes from sub-fossil remains dating from 13,000 to more than 50,000 years ago. Our results indicate that although they were similar morphologically to the extant grey wolf, dire wolves were a highly divergent lineage that split from living canids around 5.7 million years ago. In contrast to numerous examples of hybridization across Canidae2,3, there is no evidence for gene flow between dire wolves and either North American grey wolves or coyotes. This suggests that dire wolves evolved in isolation from the Pleistocene ancestors of these species. Our results also support an early New World origin of dire wolves, while the ancestors of grey wolves, coyotes and dholes evolved in Eurasia and colonized North America only relatively recently.

Data availability

The reads generated for this study have been deposited in the European Nucleotide Archive (ENA) (project number PRJEB31639). The accession numbers for the publicly available genomes used in this study can be found in Supplementary Table 2 and Supplementary Data 13. The mass-spectrometry proteomics data have been deposited in the ProteomeXchange Consortium via the PRIDE partner repository (PXD021930). Ancient collagen consensus sequences for the dire wolf can be found in Supplementary Data 17. Two-dimensional mandibular and dental shape (geometric morphometric) data have been deposited in Dryad (https://doi.org/10.5061/dryad.63xsj3v16).

References

  1. 1.

    Dundas, R. G. Quaternary records of the dire wolf, Canis dirus, in North and South America. Boreas 28, 375–385 (1999).

    Article 

    Google Scholar

  2. 2.

    vonHoldt, B. M. et al. Whole-genome sequence analysis shows that two endemic species of North American wolf are admixtures of the coyote and gray wolf. Sci. Adv. 2, e1501714 (2016).

    ADS 
    Article 

    Google Scholar

  3. 3.

    Gopalakrishnan, S. et al. Interspecific gene flow shaped the evolution of the genus Canis. Curr. Biol. 28, 3441–3449 (2018).

    CAS 
    Article 

    Google Scholar

  4. 4.

    Meachen, J. A., Brannick, A. L. & Fry, T. J. Extinct Beringian wolf morphotype found in the continental U.S. has implications for wolf migration and evolution. Ecol. Evol. 6, 3430–3438 (2016).

    Article 

    Google Scholar

  5. 5.

    Leonard, J. A. et al. Megafaunal extinctions and the disappearance of a specialized wolf ecomorph. Curr. Biol. 17, 1146–1150 (2007).

    CAS 
    Article 

    Google Scholar

  6. 6.

    Kurtén, B. & Anderson, E. Pleistocene Mammals of North America (Columbia Univ. Press, 1980).

  7. 7.

    Tedford, R. H., Wang, X. & Taylor, B. E. Phylogenetic systematics of the North American fossil Caninae (Carnivora: Canidae). Bull. Am. Nat. Hist. 325, 1–218 (2009).

    Article 

    Google Scholar

  8. 8.

    Prevosti, F. J. Phylogeny of the large extinct South American Canids (Mammalia, Carnivora, Canidae) using a ‘total evidence’ approach. Cladistics 26, 456–481 (2010).

    Article 

    Google Scholar

  9. 9.

    Zrzavý, J., Duda, P., Robovský, J., Okřinová, I. & Pavelková Řičánková, V. Phylogeny of the Caninae (Carnivora): combining morphology, behaviour, genes and fossils. Zool. Scr. 47, 373–389 (2018).

    Article 

    Google Scholar

  10. 10.

    Álvarez-Carretero, S., Goswami, A., Yang, Z. & Dos Reis, M. Bayesian estimation of species divergence times using correlated quantitative characters. Syst. Biol. 68, 967–986 (2019).

    Article 

    Google Scholar

  11. 11.

    Goulet, G. D. Comparison of temporal and geographical skull variation among Nearctic modern, Holocene and Late Pleistocene gray wolves (Canis lupus) (and selected Canis). (1993).

  12. 12.

    Graham, R. W. & Mead, J. I. in North America and Adjacent Oceans During the Last Deglaciation (eds Ruddiman, Q. F. & Wright, H. E. Jr.) 371–402 (Geological Society of America, 1987).

  13. 13.

    Barnosky, A. D. in Mass Extinctions: Processes and Evidence (ed. Donovan, S. K.) 235–254 (Belhaven, 1989).

  14. 14.

    DeSantis, L. R. G. et al. Causes and consequences of pleistocene megafaunal extinctions as revealed from Rancho La Brea mammals. Curr. Biol. 29, 2488–2495 (2019).

    CAS 
    Article 

    Google Scholar

  15. 15.

    Merriam, J. C. Note on the systematic position of the wolves of the Canis dirus group. Bull. Dept. Geol. Univ. California 10, 531–533 (1918).


    Google Scholar

  16. 16.

    Buckley, M., Harvey, V. L. & Chamberlain, A. T. Species identification and decay assessment of Late Pleistocene fragmentary vertebrate remains from Pin Hole Cave (Creswell Crags, UK) using collagen fingerprinting. Boreas 46, 402–411 (2017).

    Article 

    Google Scholar

  17. 17.

    Koepfli, K.-P. et al. Genome-wide evidence reveals that African and Eurasian golden jackals are distinct species. Curr. Biol. 25, 2158–2165 (2015).

    CAS 
    Article 

    Google Scholar

  18. 18.

    Bryant, D., Bouckaert, R., Felsenstein, J., Rosenberg, N. A. & RoyChoudhury, A. Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis. Mol. Biol. Evol. 29, 1917–1932 (2012).

    CAS 
    Article 

    Google Scholar

  19. 19.

    Yang, Z. The BPP program for species tree estimation and species delimitation. Curr. Zool. 61, 854–865 (2015).

    Article 

    Google Scholar

  20. 20.

    Geraads, D. A revision of the fossil Canidae (Mammalia) of north-western Africa. Palaeontology 54, 429–446 (2011).

    Article 

    Google Scholar

  21. 21.

    Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).

    CAS 
    Article 

    Google Scholar

  22. 22.

    vonHoldt, B. M. et al. A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res. 21, 1294–1305 (2011).

    CAS 
    Article 

    Google Scholar

  23. 23.

    Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012).

    Article 

    Google Scholar

  24. 24.

    Sinding, M. S. et al. Arctic-adapted dogs emerged at the Pleistocene–Holocene transition. Science 368, 1495–1499 (2020).

    ADS 
    CAS 
    Article 

    Google Scholar

  25. 25.

    Ní Leathlobhair, M. et al. The evolutionary history of dogs in the Americas. Science 361, 81–85 (2018).

    ADS 
    Article 

    Google Scholar

  26. 26.

    Frantz, L. A. F. et al. Genomic and archaeological evidence suggest a dual origin of domestic dogs. Science 352, 1228–1231 (2016).

    ADS 
    CAS 
    Article 

    Google Scholar

  27. 27.

    Skoglund, P., Ersmark, E., Palkopoulou, E. & Dalén, L. Ancient wolf genome reveals an early divergence of domestic dog ancestors and admixture into high-latitude breeds. Curr. Biol. 25, 1515–1519 (2015).

    CAS 
    Article 

    Google Scholar

  28. 28.

    Nowak, R. M. North American quaternary Canis. Monograph of the Museum of Natural History (Univ. Kansas, 1979).

  29. 29.

    Nowak, R. M. in Wolves: Behavior, Ecology, and Conservation (eds. Mech, L. D. & Boitani, L.) 239–258 (Univ. Chicago Press, 2003).

  30. 30.

    Sotnikova, M. & Rook, L. Dispersal of the Canini (Mammalia, Canidae: Caninae) across Eurasia during the Late Miocene to Early Pleistocene. Quat. Int. 212, 86–97 (2010).

    Article 

    Google Scholar

  31. 31.

    Saunders, J. J., Styles, B. W. & Baryshnikov, G. F. Quaternary Paleozoology in the Northern Hemisphere (Illinois State Museum, 1998).

  32. 32.

    Cooper, A. et al. Abrupt warming events drove Late Pleistocene Holarctic megafaunal turnover. Science 349, 602–606 (2015).

    ADS 
    CAS 
    Article 

    Google Scholar

  33. 33.

    Schubert, B. W. Late Quaternary chronology and extinction of North American giant short-faced bears (Arctodus simus). Quat. Int. 217, 188–194 (2010).

    Article 

    Google Scholar

  34. 34.

    Schweizer, R. M. et al. Natural selection and origin of a melanistic allele in North American gray wolves. Mol. Biol. Evol. 35, 1190–1209 (2018).

    CAS 
    Article 

    Google Scholar

  35. 35.

    Anderson, T. M. et al. Molecular and evolutionary history of melanism in North American gray wolves. Science 323, 1339–1343 (2009).

    ADS 
    CAS 
    Article 

    Google Scholar

  36. 36.

    IUCN. The IUCN Red List of Threatened Species version 2019-2 https://www.iucnredlist.org (2019).

  37. 37.

    R Core Team. R: A Language and Environment for Statistical Computing http://www.R-project.org/ (R Foundation for Statistical Computing, 2013).

Download references

Acknowledgements

We thank the staff at the Carnegie Museum of Natural History, Cincinnati Museum Center, Danish Zoological Museum, Harrison Zoological Museum, Harvard Museum of Comparative Zoology, Idaho Museum of Natural History, Institute of Archaeology (Russian Academy of Sciences), Institute of Systematics and Animal Ecology (Russian Academy of Sciences), Institute of Zoology (Chinese Academy of Sciences), Instituto de Conservação da Natureza e das Florestas, Kansas Museum of Natural History, La Brea Tar Pits and Museum, Ludwig Maximilian University, McClung Museum, Museum of the Institute of Plant and Animal Ecology (Russian Academy of Sciences), Museum national d’Histoire naturelle, National Museums Scotland, Natural History Museum London, Naturalis Biodiversity Center, Naturhistorisches Museum Bern, Smithsonian National Museum of Natural History, Swedish Naturhistoriska Riksmuseet, SYLVATROP, US Bureau of Reclamation, University of California Museum of Paleontology, University of Texas at El Paso, University of Washington Burke Museum and the Zoological Institute (Russian Academy of Sciences; state assignment no. АААА-А19-119032590102-7) for access to specimens in their care; T. Barnosky, S. Bray, A. Farrell, R. Fischer, A. Harris, J. Harris, A. Henrici, P. Holroyd, R. MacPhee, T. Martin, A. Philpot, J. Saunders, J. Southon, G. Storrs, G. Takeuchi, X. Wang and C. Widga for assistance; and L. DeSantis for comments. A.M. used computational and storage services associated with the Hoffman2 Shared Cluster provided by UCLA Institute for Digital Research and Education’s Research Technology Group. DireGWC was sequenced using the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH S10 OD018174 Instrumentation Grant. We acknowledge the assistance of the Danish National High-Throughput Sequencing Centre, BGI-Europe, the Garvan Institute of Medical Research and the Australian Cancer Research Foundation (ACRF) Cancer Genomics Facility for assistance in Illumina and BGIseq500 data generation. A.R.P. was supported by a Marie Curie COFUND Junior Research Fellowship (Durham University). A.M. was supported by an NSF grant (award number: 1457106) and the QCB Collaboratory Postdoctoral Fellowship (UCLA). L.A.F.F., J.H., A.H.-B. and G.L. were supported by either European Research Council grant (ERC-2013-StG-337574-UNDEAD and ERC-2019-StG-853272-PALAEOFARM) and/or Natural Environmental Research Council grants (NE/K005243/1 and NE/K003259/1). K.S. was supported by a grant from Barrett, the Honors College at Arizona State University. A.T.O. was supported by the Strategic Initiative Funds, Office of the President, Arizona State University to the Institute of Human Origins DNA and Human Origins at Arizona State University project. L.A.F.F. was supported by a Junior Research Fellowship (Wolfson College, University of Oxford) and L.A.F.F. and A. Carmagnini were supported by the Wellcome Trust (210119/Z/18/Z). S.G. was supported by Carlsbergfondet grant CF14–0995 and Marie Skłodowska-Curie Actions grant 655732-WhereWolf. M.T.P.G. was supported by ERC Consolidator grant 681396-Extinction Genomics. B.S. and J.K. were supported by IMLS MG-30-17-0045-17 and NSF DEB-1754451. A.H.-B. was supported by the Leverhulme Trust (ECF-2017-315). A. Cooper, K.J.M. and H.H. were supported by the Australian Research Council. A.T.S. and G.G. were supported by Australian Government Research Training Program Scholarships. A.T.L. was supported by the Peter Buck Postdoctoral Fellowship from the Smithsonian Institution’s National Museum of Natural History. Y.V.K. was supported by the by State Assignment of the Sobolev Institute of Geology and Mineralogy.

Author information

Author notes

  1. These authors contributed equally: Angela R. Perri, Kieren J. Mitchell, Alice Mouton, Sandra Álvarez-Carretero

Affiliations

  1. Department of Archaeology, Durham University, Durham, UK

    Angela R. Perri

  2. Australian Centre for Ancient DNA, School of Biological Sciences, University of Adelaide, Adelaide, South Australia, Australia

    Kieren J. Mitchell, Graham Gower, Holly Heiniger & Alexander T. Salis

  3. Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, USA

    Alice Mouton, Colin Shew, Blaire Van Valkenburgh & Robert K. Wayne

  4. School of Biological and Chemical Sciences, Queen Mary University of London, London, UK

    Sandra Álvarez-Carretero, Alberto Carmagnini, Mario dos Reis & Laurent A. F. Frantz

  5. Department of Archaeology, Classics and Egyptology, University of Liverpool, Liverpool, UK

    Ardern Hulme-Beaman & Keith Dobney

  6. School of Natural Sciences and Psychology, Liverpool John Moores University, Liverpool, UK

    Ardern Hulme-Beaman

  7. The Palaeogenomics & Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, The University of Oxford, Oxford, UK

    James Haile, Alexandra Jamieson, Audrey T. Lin, Anna Linderholm & Greger Larson

  8. Department of Anatomy, Des Moines University, Des Moines, IA, USA

    Julie Meachen

  9. Department of Zoology, University of Oxford, Oxford, UK

    Audrey T. Lin

  10. Department of Anthropology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

    Audrey T. Lin

  11. Center of Excellence in Paleontology & Department of Geosciences, East Tennessee State University, Johnson City, TN, USA

    Blaine W. Schubert

  12. Department of Archaeology, University of Exeter, Exeter, UK

    Carly Ameen

  13. Institute of Archaeology, Russian Academy of Sciences, Moscow, Russia

    Ekaterina E. Antipina

  14. ARAID Foundation, Instituto Universitario de Investigación en Ciencias Ambientales (IUCA) – Aragosaurus Group, Universidad de Zaragoza, Zaragoza, Spain

    Pere Bover

  15. Department of Earth Sciences, Natural History Museum, London, UK

    Selina Brace

  16. Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark

    Christian Carøe, Jose A. Samaniego Castruita, Shyam Gopalakrishnan, Matthew J. Collins, Mikkel-Holger S. Sinding & M. Thomas P. Gilbert

  17. Applied Paleoscience, Bothell, WA, USA

    James C. Chatters

  18. Department of Archaeology, University of Sydney, Sydney, New South Wales, Australia

    Keith Dobney

  19. Department of Archaeology, University of Aberdeen, Aberdeen, UK

    Keith Dobney

  20. Department of Archaeology, Simon Fraser University, Burnaby, Canada

    Keith Dobney

  21. Institut des Sciences de l’Evolution – Montpellier, CNRS, Université de Montpellier, IRD, EPHE, Montpellier, France

    Allowen Evin

  22. Laboratoire Evolution & Diversité Biologique, UPS/CNRS/IRD, Université Paul Sabatier, Toulouse, France

    Philippe Gaubert

  23. Australian Museum Research Institute, Australian Museum, Sydney, New South Wales, Australia

    Kristofer M. Helgen

  24. Department of Ecology and Evolutionary Biology, University of California Santa Cruz, Santa Cruz, CA, USA

    Josh Kapp, Nedda F. Saremi & Beth Shapiro

  25. Institute of Plant and Animal Ecology, Urals Branch of the Russian Academy of Sciences, Yekaterinburg, Russia

    Pavel A. Kosintsev

  26. Ural Federal University, Yekaterinburg, Russia

    Pavel A. Kosintsev

  27. Department of Anthropology, Texas A&M University, College Station, TX, USA

    Anna Linderholm

  28. Center for Evolution and Medicine, Arizona State University, Tempe, AZ, USA

    Andrew T. Ozga & Anne C. Stone

  29. School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, USA

    Andrew T. Ozga, Katherine Skerry & Anne C. Stone

  30. Halmos College of Arts and Sciences, Nova Southeastern University, Fort Lauderdale, FL, USA

    Andrew T. Ozga

  31. Department of Archaeology, University of York, York, UK

    Samantha Presslee

  32. Institute of Systematics and Ecology of Animals, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia

    Dmitry E. Taranenko

  33. Idaho Museum of Natural History, Idaho State University, Pocatello, ID, USA

    Mary Thompson

  34. Zoological Institute of the Russian Academy of Sciences, St Petersburg, Russia

    Mikhail V. Sablin

  35. Sobolev Institute of Geology and Mineralogy, Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia

    Yaroslav V. Kuzmin

  36. Tomsk State University, Tomsk, Russia

    Yaroslav V. Kuzmin

  37. McDonald Institute for Archaeological Research, University of Cambridge, Cambridge, UK

    Matthew J. Collins

  38. Greenland Institute of Natural Resources, Nuuk, Greenland

    Mikkel-Holger S. Sinding

  39. NTNU University Museum, Trondheim, Norway

    M. Thomas P. Gilbert

  40. Institute of Human Origins, Arizona State University, Tempe, AZ, USA

    Anne C. Stone

  41. Howard Hughes Medical Institute, University of California Santa Cruz, Santa Cruz, CA, USA

    Beth Shapiro

  42. South Australian Museum, Adelaide, South Australia, Australia

    Alan Cooper

  43. Palaeogenomics Group, Department of Veterinary Sciences, Ludwig Maximilian University, Munich, Germany

    Laurent A. F. Frantz

Contributions

A.R.P., K.J.M., A.M., R.K.W., G.L., L.A.F.F. and A. Cooper conceived the project and designed the research; A.R.P. and K.J.M. coordinated the sample collection efforts with input from R.K.W., G.L., L.A.F.F. and A. Cooper; A.R.P., K.J.M., A.H.-B., J.M., C.A., J.C.C., A.E., P.G., J.K., A.L., A.T.O., S.P., B.W.S., M.T., M.J.C., M.-H.S.S., M.T.P.G., A.C.S., B.S., B.V.V., R.W.K. and A. Cooper provided and/or collected samples; A.R.P., K.J.M., R.K.W., A.M., C.S., J.H., A.J., A.T.S., P.B. and H.H. conducted the genomic laboratory work; K.J.M., A.M., G.G., G.L., L.A.F.F. and A. Cooper conducted the analyses of the genomic data; S.A.-C., A.H.-B., J.M., C.A., K.M.H., and A.E. conducted the morphological analyses; A.R.P., K.J.M., A.M., S.A.-C., B.V.V., K.M.H., R.K.W., G.L., L.A.F.F. and A. Cooper wrote the paper with input from all other authors.

Corresponding authors

Correspondence to
Angela R. Perri or Kieren J. Mitchell or Laurent A. F. Frantz.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature thanks Larisa DeSantis and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Discussion, Supplementary Figures 1-23, and Supplementary Tables 1-11.

Supplementary Data

This file contains Supplementary Data 1-16.

Supplementary Data

This file contains the collagen amino sequence of the dire wolf in a fasta format.

About this article

Verify currency and authenticity via CrossMark

Cite this article

Perri, A.R., Mitchell, K.J., Mouton, A. et al. Dire wolves were the last of an ancient New World canid lineage.
Nature (2021). https://doi.org/10.1038/s41586-020-03082-x

Download citation

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

About the author

Add Comment

By 1

Get in touch