Genomes of Pleistocene Siberian Wolves Uncover Multiple Extinct Wolf Lineages

doi:10.1016/j.cub.2020.10.002

. 2021 Jan 11;31(1):198-206.e8.

doi: 10.1016/j.cub.2020.10.002. Epub 2020 Oct 29.

Genomes of Pleistocene Siberian Wolves Uncover Multiple Extinct Wolf Lineages

Jazmín Ramos-Madrigal¹, Mikkel-Holger S Sinding², Christian Carøe³, Sarah S T Mak¹, Jonas Niemann³, José A Samaniego Castruita³, Sergey Fedorov⁴, Alexander Kandyba⁵, Mietje Germonpré⁶, Hervé Bocherens⁷, Tatiana R Feuerborn⁸, Vladimir V Pitulko⁹, Elena Y Pavlova¹⁰, Pavel A Nikolskiy¹¹, Aleksei K Kasparov⁹, Varvara V Ivanova¹², Greger Larson¹³, Laurent A F Frantz¹⁴, Eske Willerslev¹⁵, Morten Meldgaard¹⁶, Bent Petersen¹⁷, Thomas Sicheritz-Ponten¹⁷, Lutz Bachmann¹⁸, Øystein Wiig¹⁸, Anders J Hansen⁸, M Thomas P Gilbert¹⁹, Shyam Gopalakrishnan²⁰

Affiliations

¹ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
² Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Natural History Museum, University of Oslo, Oslo, Norway; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; Greenland Institute of Natural Resources, Nuuk, Greenland; Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland.
³ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
⁴ Mammoth Museum of North-Eastern Federal University, Yakutsk, Russia.
⁵ Department of Stone Age Archeology, Institute of Archaeology and Ethnography of the Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia.
⁶ Directorate Earth and History of Life, Royal Belgian Institute of Natural Sciences, Brussels, Belgium.
⁷ Department of Geosciences, Biogeology, University of Tübingen, Tübingen, Germany; Senckenberg Centre for Human Evolution and Palaeoenvironment, Tübingen, Germany.
⁸ Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; Section for GeoGenetics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
⁹ Institute for the History of Material Culture, Russian Academy of Sciences, St. Petersburg, Russia.
¹⁰ Arctic and Antarctic Research Institute, St. Petersburg, Russia.
¹¹ Geological Institute, Russian Academy of Sciences, Moscow, Russia.
¹² VNIIOkeangeologia Research Institute (The All-Russian Research Institute of Geology and Mineral Resources of the World Ocean), St. Petersburg, Russia.
¹³ The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK.
¹⁴ School of Biological and Chemical Sciences, Queen Mary University of London, London, UK; Palaeogenomics Group, Department of Veterinary Sciences, Ludwig Maximilian University, Munich, Germany.
¹⁵ Section for GeoGenetics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Danish Institute for Advanced Study (D-IAS), University of Southern Denmark, Odense, Denmark; Department of Zoology, University of Cambridge, Cambridge, UK; Wellcome Trust Sanger Institute, University of Cambridge, Cambridge, UK.
¹⁶ The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; Section for GeoGenetics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
¹⁷ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Centre of Excellence for Omics-Driven Computational Biodiscovery (COMBio), Faculty of Applied Sciences, AIMST University, Kedah, Malaysia.
¹⁸ Natural History Museum, University of Oslo, Oslo, Norway.
¹⁹ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; University Museum, Norwegian University of Science and Technology, Trondheim, Norway.
²⁰ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Bioinformatics, Department of Health Technology, Technical University of Denmark, Lyngby, Denmark. Electronic address: [email protected].

PMID: 33125870
PMCID: PMC7809626
DOI: 10.1016/j.cub.2020.10.002

Genomes of Pleistocene Siberian Wolves Uncover Multiple Extinct Wolf Lineages

Jazmín Ramos-Madrigal et al. Curr Biol. 2021.

. 2021 Jan 11;31(1):198-206.e8.

doi: 10.1016/j.cub.2020.10.002. Epub 2020 Oct 29.

Authors

Affiliations

¹ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
² Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Natural History Museum, University of Oslo, Oslo, Norway; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; Greenland Institute of Natural Resources, Nuuk, Greenland; Smurfit Institute of Genetics, Trinity College Dublin, Dublin, Ireland.
³ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
⁴ Mammoth Museum of North-Eastern Federal University, Yakutsk, Russia.
⁵ Department of Stone Age Archeology, Institute of Archaeology and Ethnography of the Siberian Branch of the Russian Academy of Sciences, Novosibirsk, Russia.
⁶ Directorate Earth and History of Life, Royal Belgian Institute of Natural Sciences, Brussels, Belgium.
⁷ Department of Geosciences, Biogeology, University of Tübingen, Tübingen, Germany; Senckenberg Centre for Human Evolution and Palaeoenvironment, Tübingen, Germany.
⁸ Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; Section for GeoGenetics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
⁹ Institute for the History of Material Culture, Russian Academy of Sciences, St. Petersburg, Russia.
¹⁰ Arctic and Antarctic Research Institute, St. Petersburg, Russia.
¹¹ Geological Institute, Russian Academy of Sciences, Moscow, Russia.
¹² VNIIOkeangeologia Research Institute (The All-Russian Research Institute of Geology and Mineral Resources of the World Ocean), St. Petersburg, Russia.
¹³ The Palaeogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, Oxford, UK.
¹⁴ School of Biological and Chemical Sciences, Queen Mary University of London, London, UK; Palaeogenomics Group, Department of Veterinary Sciences, Ludwig Maximilian University, Munich, Germany.
¹⁵ Section for GeoGenetics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Danish Institute for Advanced Study (D-IAS), University of Southern Denmark, Odense, Denmark; Department of Zoology, University of Cambridge, Cambridge, UK; Wellcome Trust Sanger Institute, University of Cambridge, Cambridge, UK.
¹⁶ The Qimmeq Project, University of Greenland, Nuussuaq, Greenland; Section for GeoGenetics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
¹⁷ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Centre of Excellence for Omics-Driven Computational Biodiscovery (COMBio), Faculty of Applied Sciences, AIMST University, Kedah, Malaysia.
¹⁸ Natural History Museum, University of Oslo, Oslo, Norway.
¹⁹ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; University Museum, Norwegian University of Science and Technology, Trondheim, Norway.
²⁰ Section for Evolutionary Genomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Center for Evolutionary Hologenomics, The GLOBE Institute, University of Copenhagen, Copenhagen, Denmark; Bioinformatics, Department of Health Technology, Technical University of Denmark, Lyngby, Denmark. Electronic address: [email protected].

PMID: 33125870
PMCID: PMC7809626
DOI: 10.1016/j.cub.2020.10.002

Abstract

Extant Canis lupus genetic diversity can be grouped into three phylogenetically distinct clades: Eurasian and American wolves and domestic dogs.¹ Genetic studies have suggested these groups trace their origins to a wolf population that expanded during the last glacial maximum (LGM)^1-3 and replaced local wolf populations.⁴ Moreover, ancient genomes from the Yana basin and the Taimyr peninsula provided evidence of at least one extinct wolf lineage that dwelled in Siberia during the Pleistocene.³⁵ Previous studies have suggested that Pleistocene Siberian canids can be classified into two groups based on cranial morphology. Wolves in the first group are most similar to present-day populations, although those in the second group possess intermediate features between dogs and wolves.⁶⁷ However, whether this morphological classification represents distinct genetic groups remains unknown. To investigate this question and the relationships between Pleistocene canids, present-day wolves, and dogs, we resequenced the genomes of four Pleistocene canids from Northeast Siberia dated between >50 and 14 ka old, including samples from the two morphological categories. We found these specimens cluster with the two previously sequenced Pleistocene wolves, which are genetically more similar to Eurasian wolves. Our results show that, though the four specimens represent extinct wolf lineages, they do not form a monophyletic group. Instead, each Pleistocene Siberian canid branched off the lineage that gave rise to present-day wolves and dogs. Finally, our results suggest the two previously described morphological groups could represent independent lineages similarly related to present-day wolves and dogs.

Keywords: Pleistocene Siberia; Pleistocene biodiversity; Siberian canids; ancient DNA; dog domestication; palaeogenomics; paleolithic dog; wolf genomics.

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Conflict of interest statement

Declaration of Interests The authors declare no competing interests.

Figures

**Figure 1**
Genomic Relationships between Pleistocene Canids and Present-Day Wolves and Dogs (A) Map showing the approximate geographic location of the Pleistocene canids. The genomic coverage is indicated in parentheses. ^∗Samples sequenced in this study. (B) MDS plot including new and reference samples. For each sample, we used a consensus sequence at sites with coverage ≥3 (5,057,255 transversion sites were used). (C) MDS plot excluding dogs. Colors for (B) and (C) are indicated in the (C) legend. (D) Clustering analysis using ADMIXTURE and assuming 14 ancestry components (2,387,804 transversion sites were used). Horizontal bars show different samples, colors indicate the inferred ancestry components, and the proportion of each color shows the estimated ancestry proportions. We show the six Pleistocene canids as wider bars in the rightmost side, sorted from the youngest to the oldest. See also Tables S1 and S2 and Figures S1 and S2.

**Figure 2**
F-Statistics-Based Admixture Graph Modeling the Ancestry of Ancient and Present-Day Wolves and Dogs (A) Schematic representation of the best model, including the Pleistocene canids and representative samples of relevant groups: Eurasian wolf; American wolf; dog; golden jackal; and coyote. Admixture graph was built using the haploid panel and 846,672 transversion sites. Continuous lines show phylogenetic relationships between samples with the numbers at the right side indicating the estimated genetic drift. Dotted lines represent admixture edges with the number at the left side indicating the percentage of ancestry deriving from each lineage. Samples included in the model are shown as color-coded boxes as indicated in the legend. This graph considers the gene flow between golden jackal and Eurasian wolf reported in Freedman et al.^∗This admixture edge was not recovered when using the diploid dataset. (B–E) D-statistics estimated using *qpDstat* testing the principal features of the admixture graph in (A). Points indicate the D obtained from each test. Horizontal bars indicate 1 (wider lines) and 3.33 (thinner lines) standard errors. (B) Bunge-Toll-1885 shares more alleles with the coyote than Tirekhtyakh. (C) The American wolf (Ellesmere 1) shares more alleles with Tumat 2 and Ulakhan Sular canids when compared to the rest of the samples in the graph. (D) The golden jackal shares more alleles with the wolf lineage (as represented by the >50-ka-old Tirekhtyakh canid) than with coyotes. (E) The Eurasian wolf (Portuguese wolf) forms a clade with dogs to the exclusion of all other groups in the graph (H3): points indicate the Z score obtained from each test, and names are indicated for dogs that yielded a significant Z score (|Z| > 3.33). See also Figures S3 and S4.

**Figure 3**
D-Statistic Testing for Gene Flow between Dogs and the Pleistocene Canids (A) Map showing the geographic distribution of the dogs included in the tests. (B) Graphic representation of the D-statistic test in (C). (C) D-statistic test of the form D(boxer dog, H2; Pleistocene canid, Andean fox), where H2 corresponds to all dogs in the dataset. Points indicate the D obtained from the test. Sample names are shown for tests that yielded significant results (Z ≤ 3.33), suggesting gene flow between H2 and H3. Horizontal bars indicate 3.33 standard errors. (D) Histogram of the Z scores obtained from a D-statistic of the form D(dog 1, dog 2; Pleistocene canid 1, Pleistocene canid 2), where dog 1 and 2 are all possible pairs of present-day dogs and Pleistocene canid 1 and 2 are all possible pairs of Pleistocene canids (indicated at the top of each individual histogram). Dotted black lines correspond to a Z score of 3.3 (p = ∼0.001), and dotted red lines represent a Z score of 5.198 (p = ∼0.01 after applying a Bonferroni correction for 49,813 comparisons). None of the tests yielded a significant Z score after applying the Bonferroni correction.

**Figure 4**
D-Statistic Testing for Gene Flow between Present-Day Wolves and Pleistocene Canids (A) Map showing the geographic distribution of the present-day wolves included in the tests. (B) Graphic representation of the D-statistic tests in (C) and (D). Portuguese and Ellesmere 1 wolves are used in H1 because they do not show Pleistocene wolf ancestry in the admixture graph (Figure 2A). (C) D-statistic test of the form D(Portuguese wolf, H2; Pleistocene canid, Andean fox), where H2 corresponds to all Eurasian wolves in the dataset. Only Shanxi 2 wolf yielded a Z score consistent with gene flow from 3 of the Pleistocene canids. (D) D-statistic test of the form D(Ellesmere 1 wolf, H2; ancient wolf, Andean fox), where H2 corresponds to all American wolves in the dataset. American wolves in H2 are sorted according to their proportion of coyote ancestry as identified in Gopalakrishnan et al. from the one with the smallest (top) to the largest (bottom) proportion. Points indicate the D value obtained from each test. Sample names and closed circles are shown for test that yielded significant results (|Z| ≥ 3.33). Horizontal bars indicate 3.33 standard errors in (C) and (D).

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[1] Fan Z., Silva P., Gronau I., Wang S., Armero A.S., Schweizer R.M., Ramirez O., Pollinger J., Galaverni M., Ortega Del-Vecchyo D. Worldwide patterns of genomic variation and admixture in gray wolves. Genome Res. 2016;26:163–173. - PMC - PubMed

[2] Fan Z., Silva P., Gronau I., Wang S., Armero A.S., Schweizer R.M., Ramirez O., Pollinger J., Galaverni M., Ortega Del-Vecchyo D. Worldwide patterns of genomic variation and admixture in gray wolves. Genome Res. 2016;26:163–173. - PMC - PubMed

[3] Freedman A.H., Gronau I., Schweizer R.M., Ortega-Del Vecchyo D., Han E., Silva P.M., Galaverni M., Fan Z., Marx P., Lorente-Galdos B. Genome sequencing highlights the dynamic early history of dogs. PLoS Genet. 2014;10:e1004016. - PMC - PubMed

[4] Freedman A.H., Gronau I., Schweizer R.M., Ortega-Del Vecchyo D., Han E., Silva P.M., Galaverni M., Fan Z., Marx P., Lorente-Galdos B. Genome sequencing highlights the dynamic early history of dogs. PLoS Genet. 2014;10:e1004016. - PMC - PubMed

[5] 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. 2015;25:1515–1519. - PubMed

[6] 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. 2015;25:1515–1519. - PubMed

[7] Loog L., Thalmann O., Sinding M.S., Schuenemann V.J., Perri A., Germonpré M., Bocherens H., Witt K.E., Samaniego Castruita J.A., Velasco M.S. Ancient DNA suggests modern wolves trace their origin to a Late Pleistocene expansion from Beringia. Mol. Ecol. 2020;29:1596–1610. - PMC - PubMed

[8] Loog L., Thalmann O., Sinding M.S., Schuenemann V.J., Perri A., Germonpré M., Bocherens H., Witt K.E., Samaniego Castruita J.A., Velasco M.S. Ancient DNA suggests modern wolves trace their origin to a Late Pleistocene expansion from Beringia. Mol. Ecol. 2020;29:1596–1610. - PMC - PubMed

[9] Sinding M.S., Gopalakrishnan S., Ramos-Madrigal J., de Manuel M., Pitulko V.V., Kuderna L., Feuerborn T.R., Frantz L.A.F., Vieira F.G., Niemann J. Arctic-adapted dogs emerged at the Pleistocene-Holocene transition. Science. 2020;368:1495–1499. - PMC - PubMed

[10] Sinding M.S., Gopalakrishnan S., Ramos-Madrigal J., de Manuel M., Pitulko V.V., Kuderna L., Feuerborn T.R., Frantz L.A.F., Vieira F.G., Niemann J. Arctic-adapted dogs emerged at the Pleistocene-Holocene transition. Science. 2020;368:1495–1499. - PMC - PubMed

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Genomes of Pleistocene Siberian Wolves Uncover Multiple Extinct Wolf Lineages

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Genomes of Pleistocene Siberian Wolves Uncover Multiple Extinct Wolf Lineages

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