Middle Pleistocene genome calibrates a revised evolutionary history of extinct cave bears

Axel Barlow; Johanna L.A. Paijmans; Federica Alberti; Boris Gasparyan; Guy Bar-Oz; Ron Pinhasi; Irina Foronova; Andrey Y. Puzachenko; Martina Pacher; Love Dalén; Gennady Baryshnikov; Michael Hofreiter

doi:10.1016/j.cub.2021.01.073

Middle Pleistocene genome calibrates a revised evolutionary history of extinct cave bears

Axel Barlow, Johanna L.A. Paijmans, Federica Alberti, Boris Gasparyan, Guy Bar-Oz, Ron Pinhasi, Irina Foronova, Andrey Y. Puzachenko, Martina Pacher, Love Dalén, Gennady Baryshnikov, Michael Hofreiter

Department of Archaeology

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

Abstract

Palaeogenomes provide the potential to study evolutionary processes in real time, but this potential is limited by our ability to recover genetic data over extended timescales.¹ As a consequence, most studies so far have focused on samples of Late Pleistocene or Holocene age, which covers only a small part of the history of many clades and species. Here, we report the recovery of a low coverage palaeogenome from the petrous bone of a ∼360,000 year old cave bear from Kudaro 1 cave in the Caucasus Mountains. Analysis of this genome alongside those of several Late Pleistocene cave bears reveals widespread mito-nuclear discordance in this group. Using the time interval between Middle and Late Pleistocene cave bear genomes, we directly estimate ursid nuclear and mitochondrial substitution rates to calibrate their respective phylogenies. This reveals post-divergence mitochondrial transfer as the dominant factor explaining their mito-nuclear discordance. Interestingly, these transfer events were not accompanied by large-scale nuclear introgression. However, we do detect additional instances of nuclear admixture among other cave bear lineages, and between cave bears and brown bears, which are not associated with mitochondrial exchange. Genomic data obtained from the Middle Pleistocene cave bear petrous bone has thus facilitated a revised evolutionary history of this extinct megafaunal group. Moreover, it suggests that petrous bones may provide a means of extending both the magnitude and time depth of palaeogenome retrieval over substantial portions of the evolutionary histories of many mammalian clades.

Original language	English
Pages (from-to)	1771-1779
Journal	Current Biology
Volume	31
Issue number	8
DOIs	https://doi.org/10.1016/j.cub.2021.01.073
State	Published - 26 Apr 2021

Bibliographical note

Funding Information:
We pay tribute to our coauthor Irina Foronova for her contributions to the field of paleontology, who sadly passed away prior to the publication of this study. We thank Anthony J. Stuart for his help collecting radiocarbon dates of Ural cave bears. The authors would like to acknowledge support from the Science for Life Laboratory, the National Genomics Infrastructure (NGI), Sweden, the Knut and Alice Wallenberg Foundation and UPPMAX for providing assistance in massively parallel DNA sequencing and computational infrastructure. This work was funded by European Research Council (ERC) starting grant ?gene flow? 310763 to M.H. The work was further carried out within a framework of the Federal theme of the Theriology laboratory of the Zoological Institute of the Russian Academy of Sciences no. ????-?19-119032590102-7 ?Phylogeny, morphology and systematics of placental mammals?; the project ?The evolution of the organic world. Role and influence of planetary processes (subprogram I. Development of life and biosphere processes)? (G.B.); the Federal theme of the Laboratory of Biogeography of Institute of Geography of the RAS no. ????-?19-119021990093-8 ?Evaluation of physical and geographical, hydrological, and biotic environmental changes and their effects for the base of sustainable environmental management? (A.Y.P.); supported partly by an RFBR grant to A.Y.P. (17-01-00100-?); and on the state assignment of the V.S. Sobolev Institute of Geology and Mineralogy, Siberian Branch of the RAS (I.F.). In alphabetical order: Conceptualization, A.B. G.B. and M.H.; Data curation, A.B.; Formal analysis, A.B. and J.L.A.P.; Funding acquisition, M.H.; Investigation, F.A. and M.P.; Methodology, A.B.; Project administration, A.B. L.D. and M.H.; Resources, B.G. E.B. G.B. G.B.-O. I.F. L.D. and R.P.; Software, A.B. and J.L.A.P.; Supervision, A.B. A.Y.P. G.B. and M.H.; Validation, A.B. and J.L.A.P.; Visualization, A.B.; Writing ? original draft, A.B.; Writing ? review & editing, all authors. The authors declare no competing interests.

Publisher Copyright:
© 2021 Elsevier Inc.

Keywords

Middle Pleistocene
Ursus
ancient DNA
cave bear
evolution
paleogenomics

ASJC Scopus subject areas

General Neuroscience
General Biochemistry, Genetics and Molecular Biology
General Agricultural and Biological Sciences

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10.1016/j.cub.2021.01.073

Cite this

@article{faef52fb42b143db93a3145ccc1d6384,

title = "Middle Pleistocene genome calibrates a revised evolutionary history of extinct cave bears",

abstract = "Palaeogenomes provide the potential to study evolutionary processes in real time, but this potential is limited by our ability to recover genetic data over extended timescales.1 As a consequence, most studies so far have focused on samples of Late Pleistocene or Holocene age, which covers only a small part of the history of many clades and species. Here, we report the recovery of a low coverage palaeogenome from the petrous bone of a ∼360,000 year old cave bear from Kudaro 1 cave in the Caucasus Mountains. Analysis of this genome alongside those of several Late Pleistocene cave bears reveals widespread mito-nuclear discordance in this group. Using the time interval between Middle and Late Pleistocene cave bear genomes, we directly estimate ursid nuclear and mitochondrial substitution rates to calibrate their respective phylogenies. This reveals post-divergence mitochondrial transfer as the dominant factor explaining their mito-nuclear discordance. Interestingly, these transfer events were not accompanied by large-scale nuclear introgression. However, we do detect additional instances of nuclear admixture among other cave bear lineages, and between cave bears and brown bears, which are not associated with mitochondrial exchange. Genomic data obtained from the Middle Pleistocene cave bear petrous bone has thus facilitated a revised evolutionary history of this extinct megafaunal group. Moreover, it suggests that petrous bones may provide a means of extending both the magnitude and time depth of palaeogenome retrieval over substantial portions of the evolutionary histories of many mammalian clades.",

keywords = "Middle Pleistocene, Ursus, ancient DNA, cave bear, evolution, paleogenomics",

author = "Axel Barlow and Paijmans, {Johanna L.A.} and Federica Alberti and Boris Gasparyan and Guy Bar-Oz and Ron Pinhasi and Irina Foronova and Puzachenko, {Andrey Y.} and Martina Pacher and Love Dal{\'e}n and Gennady Baryshnikov and Michael Hofreiter",

note = "Funding Information: We pay tribute to our coauthor Irina Foronova for her contributions to the field of paleontology, who sadly passed away prior to the publication of this study. We thank Anthony J. Stuart for his help collecting radiocarbon dates of Ural cave bears. The authors would like to acknowledge support from the Science for Life Laboratory, the National Genomics Infrastructure (NGI), Sweden, the Knut and Alice Wallenberg Foundation and UPPMAX for providing assistance in massively parallel DNA sequencing and computational infrastructure. This work was funded by European Research Council (ERC) starting grant ?gene flow? 310763 to M.H. The work was further carried out within a framework of the Federal theme of the Theriology laboratory of the Zoological Institute of the Russian Academy of Sciences no. ????-?19-119032590102-7 ?Phylogeny, morphology and systematics of placental mammals?; the project ?The evolution of the organic world. Role and influence of planetary processes (subprogram I. Development of life and biosphere processes)? (G.B.); the Federal theme of the Laboratory of Biogeography of Institute of Geography of the RAS no. ????-?19-119021990093-8 ?Evaluation of physical and geographical, hydrological, and biotic environmental changes and their effects for the base of sustainable environmental management? (A.Y.P.); supported partly by an RFBR grant to A.Y.P. (17-01-00100-?); and on the state assignment of the V.S. Sobolev Institute of Geology and Mineralogy, Siberian Branch of the RAS (I.F.). In alphabetical order: Conceptualization, A.B. G.B. and M.H.; Data curation, A.B.; Formal analysis, A.B. and J.L.A.P.; Funding acquisition, M.H.; Investigation, F.A. and M.P.; Methodology, A.B.; Project administration, A.B. L.D. and M.H.; Resources, B.G. E.B. G.B. G.B.-O. I.F. L.D. and R.P.; Software, A.B. and J.L.A.P.; Supervision, A.B. A.Y.P. G.B. and M.H.; Validation, A.B. and J.L.A.P.; Visualization, A.B.; Writing ? original draft, A.B.; Writing ? review & editing, all authors. The authors declare no competing interests. Publisher Copyright: {\textcopyright} 2021 Elsevier Inc.",

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doi = "10.1016/j.cub.2021.01.073",

language = "English",

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AU - Paijmans, Johanna L.A.

AU - Alberti, Federica

AU - Gasparyan, Boris

AU - Bar-Oz, Guy

AU - Pinhasi, Ron

AU - Foronova, Irina

AU - Puzachenko, Andrey Y.

AU - Pacher, Martina

AU - Dalén, Love

AU - Baryshnikov, Gennady

AU - Hofreiter, Michael

N1 - Funding Information: We pay tribute to our coauthor Irina Foronova for her contributions to the field of paleontology, who sadly passed away prior to the publication of this study. We thank Anthony J. Stuart for his help collecting radiocarbon dates of Ural cave bears. The authors would like to acknowledge support from the Science for Life Laboratory, the National Genomics Infrastructure (NGI), Sweden, the Knut and Alice Wallenberg Foundation and UPPMAX for providing assistance in massively parallel DNA sequencing and computational infrastructure. This work was funded by European Research Council (ERC) starting grant ?gene flow? 310763 to M.H. The work was further carried out within a framework of the Federal theme of the Theriology laboratory of the Zoological Institute of the Russian Academy of Sciences no. ????-?19-119032590102-7 ?Phylogeny, morphology and systematics of placental mammals?; the project ?The evolution of the organic world. Role and influence of planetary processes (subprogram I. Development of life and biosphere processes)? (G.B.); the Federal theme of the Laboratory of Biogeography of Institute of Geography of the RAS no. ????-?19-119021990093-8 ?Evaluation of physical and geographical, hydrological, and biotic environmental changes and their effects for the base of sustainable environmental management? (A.Y.P.); supported partly by an RFBR grant to A.Y.P. (17-01-00100-?); and on the state assignment of the V.S. Sobolev Institute of Geology and Mineralogy, Siberian Branch of the RAS (I.F.). In alphabetical order: Conceptualization, A.B. G.B. and M.H.; Data curation, A.B.; Formal analysis, A.B. and J.L.A.P.; Funding acquisition, M.H.; Investigation, F.A. and M.P.; Methodology, A.B.; Project administration, A.B. L.D. and M.H.; Resources, B.G. E.B. G.B. G.B.-O. I.F. L.D. and R.P.; Software, A.B. and J.L.A.P.; Supervision, A.B. A.Y.P. G.B. and M.H.; Validation, A.B. and J.L.A.P.; Visualization, A.B.; Writing ? original draft, A.B.; Writing ? review & editing, all authors. The authors declare no competing interests. Publisher Copyright: © 2021 Elsevier Inc.

PY - 2021/4/26

Y1 - 2021/4/26

N2 - Palaeogenomes provide the potential to study evolutionary processes in real time, but this potential is limited by our ability to recover genetic data over extended timescales.1 As a consequence, most studies so far have focused on samples of Late Pleistocene or Holocene age, which covers only a small part of the history of many clades and species. Here, we report the recovery of a low coverage palaeogenome from the petrous bone of a ∼360,000 year old cave bear from Kudaro 1 cave in the Caucasus Mountains. Analysis of this genome alongside those of several Late Pleistocene cave bears reveals widespread mito-nuclear discordance in this group. Using the time interval between Middle and Late Pleistocene cave bear genomes, we directly estimate ursid nuclear and mitochondrial substitution rates to calibrate their respective phylogenies. This reveals post-divergence mitochondrial transfer as the dominant factor explaining their mito-nuclear discordance. Interestingly, these transfer events were not accompanied by large-scale nuclear introgression. However, we do detect additional instances of nuclear admixture among other cave bear lineages, and between cave bears and brown bears, which are not associated with mitochondrial exchange. Genomic data obtained from the Middle Pleistocene cave bear petrous bone has thus facilitated a revised evolutionary history of this extinct megafaunal group. Moreover, it suggests that petrous bones may provide a means of extending both the magnitude and time depth of palaeogenome retrieval over substantial portions of the evolutionary histories of many mammalian clades.

AB - Palaeogenomes provide the potential to study evolutionary processes in real time, but this potential is limited by our ability to recover genetic data over extended timescales.1 As a consequence, most studies so far have focused on samples of Late Pleistocene or Holocene age, which covers only a small part of the history of many clades and species. Here, we report the recovery of a low coverage palaeogenome from the petrous bone of a ∼360,000 year old cave bear from Kudaro 1 cave in the Caucasus Mountains. Analysis of this genome alongside those of several Late Pleistocene cave bears reveals widespread mito-nuclear discordance in this group. Using the time interval between Middle and Late Pleistocene cave bear genomes, we directly estimate ursid nuclear and mitochondrial substitution rates to calibrate their respective phylogenies. This reveals post-divergence mitochondrial transfer as the dominant factor explaining their mito-nuclear discordance. Interestingly, these transfer events were not accompanied by large-scale nuclear introgression. However, we do detect additional instances of nuclear admixture among other cave bear lineages, and between cave bears and brown bears, which are not associated with mitochondrial exchange. Genomic data obtained from the Middle Pleistocene cave bear petrous bone has thus facilitated a revised evolutionary history of this extinct megafaunal group. Moreover, it suggests that petrous bones may provide a means of extending both the magnitude and time depth of palaeogenome retrieval over substantial portions of the evolutionary histories of many mammalian clades.

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KW - Ursus

KW - ancient DNA

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JO - Current Biology

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ER -

Middle Pleistocene genome calibrates a revised evolutionary history of extinct cave bears

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

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