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Partial genomic survival of cave bears in living brown bears

Abstract

Although many large mammal species went extinct at the end of the Pleistocene epoch, their DNA may persist due to past episodes of interspecies admixture. However, direct empirical evidence of the persistence of ancient alleles remains scarce. Here, we present multifold coverage genomic data from four Late Pleistocene cave bears (Ursus spelaeus complex) and show that cave bears hybridized with brown bears (Ursus arctos) during the Pleistocene. We develop an approach to assess both the directionality and relative timing of gene flow. We find that segments of cave bear DNA still persist in the genomes of living brown bears, with cave bears contributing 0.9 to 2.4% of the genomes of all brown bears investigated. Our results show that even though extinction is typically considered as absolute, following admixture, fragments of the gene pool of extinct species can survive for tens of thousands of years in the genomes of extant recipient species.

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Fig. 1: Phylogenetic relationships of the sequenced brown, polar and cave bear genomes.
Fig. 2
Fig. 3: Test of gene flow direction based on the distribution of rooted tree topologies along a non-overlapping 25 kb sliding window.

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Acknowledgements

This work was funded by European Research Council (ERC) consolidator grant ‘gene flow’ 310763 to M.H. G.G.F. and R.P. were supported by ERC starting grant 263441 to R.P. A.G.-d’A. and A.G.-V. were supported by research project CGL2014-57209-P of the Spanish Ministry of Economy and Competitiveness to A.G.-d’A. J.A.C. and B.S. were supported by a grant from the Gordon and Betty Moore Foundation (GBMF-3804) and NSF ARC-1417036 to B.S. U.S. was supported by grant IUT20-32 from the Estonian Ministry of Education and Research, and P.A. by the Estonian Science Foundation DoRa programme. We thank the regional governments of Asturias and Castilla y León, in Spain, for providing tissue samples of Cantabrian bears. The authors would like to acknowledge support from 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.

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Authors and Affiliations

Authors

Contributions

A.B. and M.H. conceived the study; A.B., G.X., G.G.F., L.D. and P.A. performed laboratory work; A.B., J.A.C., S.H., C.T. and J.L.A.P. performed data analysis; A.B., J.A.C., S.H., C.T., J.L.A.P., G.X., G.B., R.P., L.D., B.S., M.S. and M.H. interpreted the results; A.B., J.A.C., S.H., C.T., J.L.A.P., B.S., M.S. and M.H. provided theoretical discussion of methodological developments; M.H., B.S. and M.S. supervised work carried out in their respective research groups; A.B., J.A.C. and M.H. wrote the manuscript; G.R., C.F., A.G.-d’A., A.G.-V., M.M., U.S., P.A., T.S., B.G., G.B.-O. and R.P. selected samples; G.B. contributed data; M.H., R.P., B.S. and A.G.-d’A. obtained funding. All authors read, gave comments and helped to revise the final version of the manuscript.

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Correspondence to Axel Barlow.

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Supplementary information

Supplementary Tables and Figures

Supplementary information, figures and tables

Reporting Summary

Supplementary Data 1

D statistic tests for unequal allele sharing between two brown or polar bears and a cave bear candidate introgressor

Supplementary Data 2

D statistic tests for unequal allele sharing between two cave bears and a polar bear or brown bear candidate introgressor

Supplementary Data 3

D statistic tests inconsistent with the species tree as a measure of clade differentiation — comparisons within European cave bears and European cave bears relative to the Caucasus cave bear kudarensis

Supplementary Data 4

D statistic tests inconsistent with the species tree as a measure of clade differentiation — comparisons polar bears relative to brown bears, and brown bears relative to polar bears

Supplementary Data 5

f estimates of cave bear ancestry in brown relative polar bears, and among polar bears

Supplementary Data 6

f estimates of brown bear ancestry in European cave bears, relative to the Caucasus cave bear kudarensis

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Barlow, A., Cahill, J.A., Hartmann, S. et al. Partial genomic survival of cave bears in living brown bears. Nat Ecol Evol 2, 1563–1570 (2018). https://doi.org/10.1038/s41559-018-0654-8

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