Dire wolves were the last of an ancient New World canid lineage

Angela R. Perri; Kieren J. Mitchell; Alice Mouton; Sandra Álvarez-Carretero; Ardern Hulme-Beaman; James Haile; Alexandra Jamieson; Julie Meachen; Audrey T. Lin; Blaine W. Schubert; Carly Ameen; Ekaterina E. Antipina; Pere Bover; Selina Brace; Alberto Carmagnini; Christian Carøe; Jose A. Samaniego Castruita; James C. Chatters; Keith Dobney; Mario dos Reis; Allowen Evin; Philippe Gaubert; Shyam Gopalakrishnan; Graham Gower; Holly Heiniger; Kristofer M. Helgen; Josh Kapp; Pavel A. Kosintsev; Anna Linderholm; Andrew T. Ozga; Samantha Presslee; Alexander T. Salis; Nedda F. Saremi; Colin Shew; Katherine Skerry; Dmitry E. Taranenko; Mary Thompson; Mikhail V. Sablin; Yaroslav V. Kuzmin; Matthew J. Collins; Mikkel Holger S. Sinding; M. Thomas P. Gilbert; Anne C. Stone; Beth Shapiro; Blaire Van Valkenburgh; Robert K. Wayne; Greger Larson; Alan Cooper; Laurent A.F. Frantz

doi:10.1038/s41586-020-03082-x

Dire wolves were the last of an ancient New World canid lineage

Angela R. Perri^*, Kieren J. Mitchell, Alice Mouton, Sandra Álvarez-Carretero, Ardern Hulme-Beaman, James Haile, Alexandra Jamieson, Julie Meachen, Audrey T. Lin, Blaine W. Schubert, Carly Ameen, Ekaterina E. Antipina, Pere Bover, Selina Brace, Alberto Carmagnini, Christian Carøe, Jose A. Samaniego Castruita, James C. Chatters, Keith Dobney, Mario dos ReisAllowen Evin, Philippe Gaubert, Shyam Gopalakrishnan, Graham Gower, Holly Heiniger, Kristofer M. Helgen, Josh Kapp, Pavel A. Kosintsev, Anna Linderholm, Andrew T. Ozga, Samantha Presslee, Alexander T. Salis, Nedda F. Saremi, Colin Shew, Katherine Skerry, Dmitry E. Taranenko, Mary Thompson, Mikhail V. Sablin, Yaroslav V. Kuzmin, Matthew J. Collins, Mikkel Holger S. Sinding, M. Thomas P. Gilbert, Anne C. Stone, Beth Shapiro, Blaire Van Valkenburgh, Robert K. Wayne, Greger Larson, Alan Cooper, Laurent A.F. Frantz

^*Corresponding author for this work

Archaeology

Research output: Contribution to journal › Article › peer-review

39 Citations (Scopus)

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 Canidae^2,3, 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.

Original language	English
Pages (from-to)	87-91
Number of pages	5
Journal	Nature
Volume	591
Issue number	7848
Early online date	13 Jan 2021
DOIs	https://doi.org/10.1038/s41586-020-03082-x
Publication status	Published - 4 Mar 2021

Bibliographical note

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.

Data Availability Statement

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).

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Perri, A. R., Mitchell, K. J., Mouton, A., Álvarez-Carretero, S., Hulme-Beaman, A., Haile, J., Jamieson, A., Meachen, J., Lin, A. T., Schubert, B. W., Ameen, C., Antipina, E. E., Bover, P., Brace, S., Carmagnini, A., Carøe, C., Samaniego Castruita, J. A., Chatters, J. C., Dobney, K., ... Frantz, L. A. F. (2021). Dire wolves were the last of an ancient New World canid lineage. Nature, 591(7848), 87-91. https://doi.org/10.1038/s41586-020-03082-x

Perri, AR, Mitchell, KJ, Mouton, A, Álvarez-Carretero, S, Hulme-Beaman, A, Haile, J, Jamieson, A, Meachen, J, Lin, AT, Schubert, BW, Ameen, C, Antipina, EE, Bover, P, Brace, S, Carmagnini, A, Carøe, C, Samaniego Castruita, JA, Chatters, JC, Dobney, K, dos Reis, M, Evin, A, Gaubert, P, Gopalakrishnan, S, Gower, G, Heiniger, H, Helgen, KM, Kapp, J, Kosintsev, PA, Linderholm, A, Ozga, AT, Presslee, S, Salis, AT, Saremi, NF, Shew, C, Skerry, K, Taranenko, DE, Thompson, M, Sablin, MV, Kuzmin, YV, Collins, MJ, Sinding, MHS, Gilbert, MTP, Stone, AC, Shapiro, B, Van Valkenburgh, B, Wayne, RK, Larson, G, Cooper, A & Frantz, LAF 2021, 'Dire wolves were the last of an ancient New World canid lineage', Nature, vol. 591, no. 7848, pp. 87-91. https://doi.org/10.1038/s41586-020-03082-x

@article{8ce3d180ec894eee8674929faf8d659e,

title = "Dire wolves were the last of an ancient New World canid lineage",

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.",

author = "Perri, {Angela R.} and Mitchell, {Kieren J.} and Alice Mouton and Sandra {\'A}lvarez-Carretero and Ardern Hulme-Beaman and James Haile and Alexandra Jamieson and Julie Meachen and Lin, {Audrey T.} and Schubert, {Blaine W.} and Carly Ameen and Antipina, {Ekaterina E.} and Pere Bover and Selina Brace and Alberto Carmagnini and Christian Car{\o}e and {Samaniego Castruita}, {Jose A.} and Chatters, {James C.} and Keith Dobney and {dos Reis}, Mario and Allowen Evin and Philippe Gaubert and Shyam Gopalakrishnan and Graham Gower and Holly Heiniger and Helgen, {Kristofer M.} and Josh Kapp and Kosintsev, {Pavel A.} and Anna Linderholm and Ozga, {Andrew T.} and Samantha Presslee and Salis, {Alexander T.} and Saremi, {Nedda F.} and Colin Shew and Katherine Skerry and Taranenko, {Dmitry E.} and Mary Thompson and Sablin, {Mikhail V.} and Kuzmin, {Yaroslav V.} and Collins, {Matthew J.} and Sinding, {Mikkel Holger S.} and Gilbert, {M. Thomas P.} and Stone, {Anne C.} and Beth Shapiro and {Van Valkenburgh}, Blaire and Wayne, {Robert K.} and Greger Larson and Alan Cooper and Frantz, {Laurent A.F.}",

note = "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 Conserva{\c c}{\~a}o 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{\textquoteright}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{\textquoteright}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 Sk{\l}odowska-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{\textquoteright}s National Museum of Natural History. Y.V.K. was supported by the by State Assignment of the Sobolev Institute of Geology and Mineralogy. ",

year = "2021",

month = mar,

day = "4",

doi = "10.1038/s41586-020-03082-x",

language = "English",

volume = "591",

pages = "87--91",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group",

number = "7848",

}

TY - JOUR

T1 - Dire wolves were the last of an ancient New World canid lineage

AU - Perri, Angela R.

AU - Mitchell, Kieren J.

AU - Mouton, Alice

AU - Álvarez-Carretero, Sandra

AU - Hulme-Beaman, Ardern

AU - Haile, James

AU - Jamieson, Alexandra

AU - Meachen, Julie

AU - Lin, Audrey T.

AU - Schubert, Blaine W.

AU - Ameen, Carly

AU - Antipina, Ekaterina E.

AU - Bover, Pere

AU - Brace, Selina

AU - Carmagnini, Alberto

AU - Carøe, Christian

AU - Samaniego Castruita, Jose A.

AU - Chatters, James C.

AU - Dobney, Keith

AU - dos Reis, Mario

AU - Evin, Allowen

AU - Gaubert, Philippe

AU - Gopalakrishnan, Shyam

AU - Gower, Graham

AU - Heiniger, Holly

AU - Helgen, Kristofer M.

AU - Kapp, Josh

AU - Kosintsev, Pavel A.

AU - Linderholm, Anna

AU - Ozga, Andrew T.

AU - Presslee, Samantha

AU - Salis, Alexander T.

AU - Saremi, Nedda F.

AU - Shew, Colin

AU - Skerry, Katherine

AU - Taranenko, Dmitry E.

AU - Thompson, Mary

AU - Sablin, Mikhail V.

AU - Kuzmin, Yaroslav V.

AU - Collins, Matthew J.

AU - Sinding, Mikkel Holger S.

AU - Gilbert, M. Thomas P.

AU - Stone, Anne C.

AU - Shapiro, Beth

AU - Van Valkenburgh, Blaire

AU - Wayne, Robert K.

AU - Larson, Greger

AU - Cooper, Alan

AU - Frantz, Laurent A.F.

N1 - 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.

PY - 2021/3/4

Y1 - 2021/3/4

N2 - 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.

AB - 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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DO - 10.1038/s41586-020-03082-x

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SN - 0028-0836

VL - 591

SP - 87

EP - 91

JO - Nature

JF - Nature

IS - 7848

ER -

Dire wolves were the last of an ancient New World canid lineage

Abstract

Bibliographical note

Data Availability Statement

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