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.
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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).
Dundas, R. G. Quaternary records of the dire wolf, Canis dirus, in North and South America. Boreas 28, 375–385 (1999).
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).
Gopalakrishnan, S. et al. Interspecific gene flow shaped the evolution of the genus Canis. Curr. Biol. 28, 3441–3449 (2018).
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).
Leonard, J. A. et al. Megafaunal extinctions and the disappearance of a specialized wolf ecomorph. Curr. Biol. 17, 1146–1150 (2007).
Kurtén, B. & Anderson, E. Pleistocene Mammals of North America (Columbia Univ. Press, 1980).
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).
Prevosti, F. J. Phylogeny of the large extinct South American Canids (Mammalia, Carnivora, Canidae) using a ‘total evidence’ approach. Cladistics 26, 456–481 (2010).
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).
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).
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).
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).
Barnosky, A. D. in Mass Extinctions: Processes and Evidence (ed. Donovan, S. K.) 235–254 (Belhaven, 1989).
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).
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).
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).
Koepfli, K.-P. et al. Genome-wide evidence reveals that African and Eurasian golden jackals are distinct species. Curr. Biol. 25, 2158–2165 (2015).
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).
Yang, Z. The BPP program for species tree estimation and species delimitation. Curr. Zool. 61, 854–865 (2015).
Geraads, D. A revision of the fossil Canidae (Mammalia) of north-western Africa. Palaeontology 54, 429–446 (2011).
Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591 (2007).
vonHoldt, B. M. et al. A genome-wide perspective on the evolutionary history of enigmatic wolf-like canids. Genome Res. 21, 1294–1305 (2011).
Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012).
Sinding, M. S. et al. Arctic-adapted dogs emerged at the Pleistocene–Holocene transition. Science 368, 1495–1499 (2020).
Ní Leathlobhair, M. et al. The evolutionary history of dogs in the Americas. Science 361, 81–85 (2018).
Frantz, L. A. F. et al. Genomic and archaeological evidence suggest a dual origin of domestic dogs. Science 352, 1228–1231 (2016).
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).
Nowak, R. M. North American quaternary Canis. Monograph of the Museum of Natural History (Univ. Kansas, 1979).
Nowak, R. M. in Wolves: Behavior, Ecology, and Conservation (eds. Mech, L. D. & Boitani, L.) 239–258 (Univ. Chicago Press, 2003).
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).
Saunders, J. J., Styles, B. W. & Baryshnikov, G. F. Quaternary Paleozoology in the Northern Hemisphere (Illinois State Museum, 1998).
Cooper, A. et al. Abrupt warming events drove Late Pleistocene Holarctic megafaunal turnover. Science 349, 602–606 (2015).
Schubert, B. W. Late Quaternary chronology and extinction of North American giant short-faced bears (Arctodus simus). Quat. Int. 217, 188–194 (2010).
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).
Anderson, T. M. et al. Molecular and evolutionary history of melanism in North American gray wolves. Science 323, 1339–1343 (2009).
IUCN. The IUCN Red List of Threatened Species version 2019-2 https://www.iucnredlist.org (2019).
R Core Team. R: A Language and Environment for Statistical Computing http://www.R-project.org/ (R Foundation for Statistical Computing, 2013).
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.
The authors declare no competing interests.
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.
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This file contains Supplementary Methods, Supplementary Discussion, Supplementary Figures 1-23, and Supplementary Tables 1-11.
This file contains Supplementary Data 1-16.
This file contains the collagen amino sequence of the dire wolf in a fasta format.
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Perri, A.R., Mitchell, K.J., Mouton, A. et al. Dire wolves were the last of an ancient New World canid lineage. Nature 591, 87–91 (2021). https://doi.org/10.1038/s41586-020-03082-x