Environmental genomics of Late Pleistocene black bears and giant short-faced bears

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Environmental genomics of Late Pleistocene black bears and giant short-faced bears
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Pedersen, Mikkel Winther
Bianca De Sanctis
Nedda F. Saremi
Sikora, Martin
Emily E. Puckett
Zhenquan Gu
Katherine L. Moon
Joshua D. Kapp
Vinner, Lasse
Zaruhi Vardanyan
Ciprian F. Ardelean
Joaquin Arroyo-Cabrales
James A. Cahill
Peter D. Heintzman
Grant Zazula
Ross D. E. MacPhee
Beth Shapiro
Richard Durbin
Willerslev, Eske

Analysis of ancient environmental DNA (eDNA) has revolutionized our ability to describe biological communities in space and time,^1–3 by allowing for parallel sequencing of DNA from all trophic levels.^4–8 However, because environmental samples contain sparse and fragmented data from multiple individuals, and often contain closely related species,⁹ the field of ancient eDNA has so far been limited to organellar genomes in its contribution to population and phylogenetic studies.⁵^,⁶^,¹⁰^,¹¹ This is in contrast to data from fossils¹²^,¹³ where full-genome studies are routine, despite these being rare and their destruction for sequencing undesirable.^14–16 Here, we report the retrieval of three low-coverage (0.03×) environmental genomes from American black bear (Ursus americanus) and a 0.04× environmental genome of the extinct giant short-faced bear (Arctodus simus) from cave sediment samples from northern Mexico dated to 16–14 thousand calibrated years before present (cal kyr BP), which we contextualize with a new high-coverage (26×) and two lower-coverage giant short-faced bear genomes obtained from fossils recovered from Yukon Territory, Canada, which date to ∼22–50 cal kyr BP. We show that the Late Pleistocene black bear population in Mexico is ancestrally related to the present-day Eastern American black bear population, and that the extinct giant short-faced bears present in Mexico were deeply divergent from the earlier Beringian population. Our findings demonstrate the ability to separately analyze genomic-scale DNA sequences of closely related species co-preserved in environmental samples, which brings the use of ancient eDNA into the era of population genomics and phylogenetics.

Originalsprog	Engelsk
Tidsskrift	Current Biology
Vol/bind	31
Udgave nummer	12
Sider (fra-til)	2728-2736.e8
Antal sider	17
ISSN	0960-9822
DOI	https://doi.org/10.1016/j.cub.2021.04.027
Status	Udgivet - 2021

Bibliografisk note

Funding Information:
We thank Richard E. Green for commenting on the manuscript. M.W.P. acknowledges support from the Carlsberg Foundation for a Carlsberg Internationalisation grant ( CF17-0275 ). B.D.S. acknowledges support from the Wellcome Trust program in Mathematical Genomics and Medicine ( WT220023 ). E.W. acknowledges support from the Lundbeck Foundation , the Wellcome Trust , the Carlsberg Foundation , Novo Foundation , and GRF EXC CRS Chair ( 44113220 ) - Cluster of Excellence “The Ocean Floor – Earth’s Uncharted Interface.” E.W. would also like to thank Illumina for their collaboration and St. John’s College, Cambridge, for providing an excellent environment for scientific thought. R.D. acknowledges support from the Wellcome Trust (grant agreement WT207492 ). The Arctodus genome sequencing was supported by NSF ICER-1850949 and NSF DEB-1754451 , and by a grant from the Gordon and Betty Moore Foundation ( GBMF 58362 ). We thank the Tr’ondek Hwech’in and placer gold mining community for their continued support and partnership with paleontological research in the Klondike goldfields.

Funding Information:
We thank Richard E. Green for commenting on the manuscript. M.W.P. acknowledges support from the Carlsberg Foundation for a Carlsberg Internationalisation grant (CF17-0275). B.D.S. acknowledges support from the Wellcome Trust program in Mathematical Genomics and Medicine (WT220023). E.W. acknowledges support from the Lundbeck Foundation, the Wellcome Trust, the Carlsberg Foundation, Novo Foundation, and GRF EXC CRS Chair (44113220) - Cluster of Excellence ?The Ocean Floor ? Earth's Uncharted Interface.? E.W. would also like to thank Illumina for their collaboration and St. John's College, Cambridge, for providing an excellent environment for scientific thought. R.D. acknowledges support from the Wellcome Trust (grant agreement WT207492). The Arctodus genome sequencing was supported by NSF ICER-1850949 and NSF DEB-1754451, and by a grant from the Gordon and Betty Moore Foundation (GBMF 58362). We thank the Tr'ondek Hwech'in and placer gold mining community for their continued support and partnership with paleontological research in the Klondike goldfields. E.W. conceived the project. E.W. R.D. B.S. M.W.P. B.D.S. and M.S. designed the research. G.Z. R.D.E.M. and C.F.A. provided samples and information about paleontological/archaeological context. M.W.P. Z.G. L.V. and Z.V. carried out ancient eDNA laboratory work. P.D.H. K.L.M. and J.D.K. carried out the fossil DNA laboratory work, with input from B.S. N.F.S. undertook the computational analysis of the fossil data with input from P.D.H. B.S. and J.A.C. B.D.S. carried out the computational analyses of the black bear genomes and environmental genomes with input from M.S. R.D. and M.W.P. E.E.P. provided data and interpretation for the black bear results. M.W.P. B.D.S. B.S. R.D. and E.W. wrote the paper and STAR Methods, with input from E.E.P. P.D.H. R.D.E.M. and all co-authors. All authors declare no competing interests.

Publisher Copyright:
© 2021 The Author(s)

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