Ancient horse genomes reveal the timing and extent of dispersals across the Bering Land Bridge

The Bering Land Bridge (BLB) last connected Eurasia and North America during the Late Pleistocene. Although the BLB would have enabled transfers of terrestrial biota in both directions, it also acted as an ecological filter whose permeability varied considerably over time. Here we explore the possible impacts of this ecological corridor on genetic diversity within, and connectivity among, populations of a once wide-ranging group, the caballine horses (Equus spp.). Using a panel of 187 mitochondrial and eight nuclear genomes recovered from present-day and extinct caballine horses sampled across the Holarctic, we found that Eurasian horse populations initially diverged from those in North America, their ancestral continent, around 1.0–0.8 million years ago. Subsequent to this split our mitochondrial DNA analysis identified two bidirectional long-range dispersals across the BLB ~875–625 and ~200–50 thousand years ago, during the Middle and Late Pleistocene. Whole genome analysis indicated low levels of gene flow between North American and Eurasian horse populations, which probably occurred as a result of these inferred dispersals. Nonetheless, mitochondrial and nuclear diversity of caballine horse populations retained strong phylogeographical structuring. Our results suggest that barriers to gene flow, currently unidentified but possibly related to habitat distribution across Beringia or ongoing evolutionary divergence, played an important role in shaping the early genetic history of caballine horses, including the ancestors of living horses within Equus ferus. © 2021 John Wiley & Sons Ltd 19-05-00477, AAAA-A19-119032590102-7; National Science Foundation, NSF: ARC-1417036; Gordon and Betty Moore Foundation, GBMF: 3804; University of California, Santa Cruz, UCSC; U.S. Bureau of Land Management, BLM; Horizon 2020 Framework Programme, H2020: 681605; Seventh Framework Programme, FP7: IEF-302617; Natural Sciences and Engineering Research Council of Canada, NSERC; Marie Curie; European Research Council, ERC; Svenska Forskningsrådet Formas: 2018-01640; Russian Foundation for Basic Research, РФФИ: 18-04-00327; Knut och Alice Wallenbergs Stiftelse; Vetenskapsrådet, VR; Science for Life Laboratory, SciLifeLab We are grateful to the placer gold mining community, the Tr’ondëk Hwëch’in First Nation, and the Vuntut Gwitchin First Nation for their collaboration and support with our research in Yukon. Tamara Pico, Sarah Crump and Paul Koch provided advice interpreting the palaeoclimate of Beringia. Data generation was supported with funds from NSF ARC-1417036, the Gordon & Betty Moore Foundation (no. 3804) and the American Wild Horse Campaign. A.O.V. was additionally supported by a UCSC Chancellor’s Dissertation Year Fellowship and the CANA Foundation. M.T. and D.G. were supported by the Russian Foundation for Basic Research (project 18-04-00327), and L.E. by a Marie-Curie Intra-European fellowship (FP7, IEF-302617). G.B. is supported by the Federal theme of Zoological Institute of the Russian Academy of Sciences no. AAAA-A19-119032590102-7. S.V. was funded by the Russian Foundation for Basic Research, Grant 19-05-00477. L.D. acknowledges support from FORMAS (project 2018-01640). D.F. was supported by the Natural Science and Engineering Research Council. P.G. and D.M. are supported by the Bureau of Land Management. We acknowledge support from Science for Life Laboratory, the Knut and Alice Wallenberg Foundation, the National Genomics Infrastructure funded by the Swedish Research Council, and Uppsala Multidisciplinary Center for Advanced Computational Science for assistance with massively parallel sequencing and access to the UPPMAX computational infrastructure. L.O. received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement 681605). We are grateful to the placer gold mining community, the Tr?ond?k Hw?ch?in First Nation, and the Vuntut Gwitchin First Nation for their collaboration and support with our research in Yukon. Tamara Pico, Sarah Crump and Paul Koch provided advice interpreting the palaeoclimate of Beringia. Data generation was supported with funds from NSF ARC-1417036, the Gordon & Betty Moore Foundation (no. 3804) and the American Wild Horse Campaign. A.O.V. was additionally supported by a UCSC Chancellor?s Dissertation Year Fellowship and the CANA Foundation. M.T. and D.G. were supported by the Russian Foundation for Basic Research (project 18-04-00327), and L.E. by a Marie-Curie Intra-European fellowship (FP7, IEF-302617). G.B. is supported by the Federal theme of Zoological Institute of the Russian Academy of Sciences no. AAAA-A19-119032590102-7. S.V. was funded by the Russian Foundation for Basic Research, Grant 19-05-00477. L.D. acknowledges support from FORMAS (project 2018-01640). D.F. was supported by the Natural Science and Engineering Research Council. P.G. and D.M. are supported by the Bureau of Land Management. We acknowledge support from Science for Life Laboratory, the Knut and Alice Wallenberg Foundation, the National Genomics Infrastructure funded by the Swedish Research Council, and Uppsala Multidisciplinary Center for Advanced Computational Science for assistance with massively parallel sequencing and access to the UPPMAX computational infrastructure. L.O. received funding from the European Research Council (ERC) under the European Union?s Horizon 2020 research and innovation programme (grant agreement 681605).