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Late Quaternary dynamics of Arctic biota from ancient environmental genomics

Late Quaternary dynamics of Arctic biota from ancient environmental genomics
Late Quaternary dynamics of Arctic biota from ancient environmental genomics

During the last glacial–interglacial cycle, Arctic biotas experienced substantial climatic changes, yet the nature, extent and rate of their responses are not fully understood1–8. Here we report a large-scale environmental DNA metagenomic study of ancient plant and mammal communities, analysing 535 permafrost and lake sediment samples from across the Arctic spanning the past 50,000 years. Furthermore, we present 1,541 contemporary plant genome assemblies that were generated as reference sequences. Our study provides several insights into the long-term dynamics of the Arctic biota at the circumpolar and regional scales. Our key findings include: (1) a relatively homogeneous steppe–tundra flora dominated the Arctic during the Last Glacial Maximum, followed by regional divergence of vegetation during the Holocene epoch; (2) certain grazing animals consistently co-occurred in space and time; (3) humans appear to have been a minor factor in driving animal distributions; (4) higher effective precipitation, as well as an increase in the proportion of wetland plants, show negative effects on animal diversity; (5) the persistence of the steppe–tundra vegetation in northern Siberia enabled the late survival of several now-extinct megafauna species, including the woolly mammoth until 3.9 ± 0.2 thousand years ago (ka) and the woolly rhinoceros until 9.8 ± 0.2 ka; and (6) phylogenetic analysis of mammoth environmental DNA reveals a previously unsampled mitochondrial lineage. Our findings highlight the power of ancient environmental metagenomics analyses to advance understanding of population histories and long-term ecological dynamics.

0028-0836
86-92
Wang, Yucheng
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Pedersen, Mikkel Winther
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Coissac, Eric
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Möller, Per
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Willerslev, Eske
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Wang, Yucheng
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Pedersen, Mikkel Winther
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Racimo, Fernando
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Lammers, Youri
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Mangerud, Jan
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Möller, Per
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Willerslev, Eske
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Wang, Yucheng, Pedersen, Mikkel Winther, Alsos, Inger Greve, De Sanctis, Bianca, Racimo, Fernando, Prohaska, Ana, Coissac, Eric, Owens, Hannah Lois, Merkel, Marie Kristine Føreid, Fernandez-Guerra, Antonio, Rouillard, Alexandra, Lammers, Youri, Alberti, Adriana, Denoeud, France, Money, Daniel, Ruter, Anthony H., McColl, Hugh, Larsen, Nicolaj Krog, Cherezova, Anna A., Fedorov, Grigory B., Haile, James, Orlando, Ludovic, Vinner, Lasse, Korneliussen, Thorfinn Sand, Beilman, David W., Bjørk, Anders A., Cao, Jialu, Dockter, Christoph, Esdale, Julie, Gusarova, Galina, Kjeldsen, Kristian K., Mangerud, Jan, Rasic, Jeffrey T., Skadhauge, Birgitte, Svendsen, John Inge, Tikhonov, Alexei, Wincker, Patrick, Xing, Yingchun, Zhang, Yubin, Edwards, Mary, Froese, Duane G., Rahbek, Carsten, Nogues, David Bravo, Holden, Philip B., Edwards, Neil R., Meltzer, David J., Kjær, Kurt H., Möller, Per and Willerslev, Eske (2021) Late Quaternary dynamics of Arctic biota from ancient environmental genomics. Nature, 600 (7887), 86-92. (doi:10.1038/s41586-021-04016-x).

Record type: Article

Abstract

During the last glacial–interglacial cycle, Arctic biotas experienced substantial climatic changes, yet the nature, extent and rate of their responses are not fully understood1–8. Here we report a large-scale environmental DNA metagenomic study of ancient plant and mammal communities, analysing 535 permafrost and lake sediment samples from across the Arctic spanning the past 50,000 years. Furthermore, we present 1,541 contemporary plant genome assemblies that were generated as reference sequences. Our study provides several insights into the long-term dynamics of the Arctic biota at the circumpolar and regional scales. Our key findings include: (1) a relatively homogeneous steppe–tundra flora dominated the Arctic during the Last Glacial Maximum, followed by regional divergence of vegetation during the Holocene epoch; (2) certain grazing animals consistently co-occurred in space and time; (3) humans appear to have been a minor factor in driving animal distributions; (4) higher effective precipitation, as well as an increase in the proportion of wetland plants, show negative effects on animal diversity; (5) the persistence of the steppe–tundra vegetation in northern Siberia enabled the late survival of several now-extinct megafauna species, including the woolly mammoth until 3.9 ± 0.2 thousand years ago (ka) and the woolly rhinoceros until 9.8 ± 0.2 ka; and (6) phylogenetic analysis of mammoth environmental DNA reveals a previously unsampled mitochondrial lineage. Our findings highlight the power of ancient environmental metagenomics analyses to advance understanding of population histories and long-term ecological dynamics.

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Accepted/In Press date: 13 September 2021
Published date: 20 October 2021
Additional Information: Funding Information: Acknowledgements We thank D. H. Mann for his detailed and constructive comments; and T. Ager, J. Austin, T. B. Brand, A. Cooper, S. Funder, M. T. P. Gilbert, T. Jørgensen, N. J. Korsgaard, S. Liu, M. Meldgaard, P. V. S. Olsen, M. L. Siggaard-Andersen, J. Stenderup, S. A. Woodroffe and staff at the GeoGenetics Sequencing Core and National Park Service-Western Arctic National Parklands for help and support. E.W. and D.J.M. thank the staff at St. John’s College, Cambridge, for providing a stimulating environment for scientific discussion of the project. E.W. thanks Illumina for collaboration. The Lundbeck Foundation GeoGenetics Centre is supported by the Carlsberg Foundation (CF18-0024), the Lundbeck Foundation (R302-2018-2155), the Novo Nordisk Foundation (NNF18SA0035006), the Wellcome Trust (UNS69906) and GRF EXC CRS Chair (44113220)—Cluster of Excellence. The PhyloNorway plant genome database is part of the Norwegian Barcode of Life Network (https://www.norbol.org) funded by the Research Council of Norway (226134/F50), the Norwegian Biodiversity Information Centre (14-14, 70184209) and The Arctic University Museum of Norway. Metabarcoding sequencing was funded by the Central Public-Interest Scientific Institution Basal Research Fund, CAFS (2017B001 and 2020A001). B.D.S. is supported by the Wellcome Trust programme in Mathematical Genomics and Medicine (WT220023); F.R. by a Villum Fonden Young Investigator award (no. 00025300); D.J.M. by the Quest Archaeological Research Fund; P.M. by the Swedish Research Council (VR); R.D. by the Wellcome Trust (WT207492); and A.R. by a Marie Skłodowska-Curie Actions Individual Fellowship (MSCA-IF, 703542) and the Research Council of Norway (KLIMAFORSK, 294929). L.O. has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (no. 681605); I.G.A. and Y.L. from the ERC under the European Union’s Horizon 2020 research and innovation programme (no. 819192). J.I.S. and J.M. are supported by the Research Council of Norway. P.B.H. and N.R.E. acknowledge NERC funding (grant NE/ P015093/1). D.W.B. was supported by a Marie Skłodowska-Curie Actions Incoming International Fellowship (MCIIF-40974). T.S.K. is funded by a Carlsberg Foundation Young Researcher Fellowship (CF19-0712).

Identifiers

Local EPrints ID: 454453
URI: http://eprints.soton.ac.uk/id/eprint/454453
ISSN: 0028-0836
PURE UUID: 546e2766-739a-4ec2-ba23-fcb89d8518ea
ORCID for Mary Edwards: ORCID iD orcid.org/0000-0002-3490-6682

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Date deposited: 10 Feb 2022 17:30
Last modified: 18 Mar 2024 02:55

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Contributors

Author: Yucheng Wang
Author: Mikkel Winther Pedersen
Author: Inger Greve Alsos
Author: Bianca De Sanctis
Author: Fernando Racimo
Author: Ana Prohaska
Author: Eric Coissac
Author: Hannah Lois Owens
Author: Marie Kristine Føreid Merkel
Author: Antonio Fernandez-Guerra
Author: Alexandra Rouillard
Author: Youri Lammers
Author: Adriana Alberti
Author: France Denoeud
Author: Daniel Money
Author: Anthony H. Ruter
Author: Hugh McColl
Author: Nicolaj Krog Larsen
Author: Anna A. Cherezova
Author: Grigory B. Fedorov
Author: James Haile
Author: Ludovic Orlando
Author: Lasse Vinner
Author: Thorfinn Sand Korneliussen
Author: David W. Beilman
Author: Anders A. Bjørk
Author: Jialu Cao
Author: Christoph Dockter
Author: Julie Esdale
Author: Galina Gusarova
Author: Kristian K. Kjeldsen
Author: Jan Mangerud
Author: Jeffrey T. Rasic
Author: Birgitte Skadhauge
Author: John Inge Svendsen
Author: Alexei Tikhonov
Author: Patrick Wincker
Author: Yingchun Xing
Author: Yubin Zhang
Author: Mary Edwards ORCID iD
Author: Duane G. Froese
Author: Carsten Rahbek
Author: David Bravo Nogues
Author: Philip B. Holden
Author: Neil R. Edwards
Author: David J. Meltzer
Author: Kurt H. Kjær
Author: Per Möller
Author: Eske Willerslev

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