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Research Article

Fossil and genomic evidence constrains the timing of bison arrival in North America

View ORCID ProfileDuane Froese, Mathias Stiller, View ORCID ProfilePeter D. Heintzman, View ORCID ProfileAlberto V. Reyes, Grant D. Zazula, View ORCID ProfileAndré E. R. Soares, Matthias Meyer, Elizabeth Hall, Britta J. L. Jensen, Lee J. Arnold, View ORCID ProfileRoss D. E. MacPhee, and View ORCID ProfileBeth Shapiro
PNAS March 28, 2017 114 (13) 3457-3462; first published March 13, 2017; https://doi.org/10.1073/pnas.1620754114
Duane Froese
aDepartment of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, Canada T6G 2E3;
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  • ORCID record for Duane Froese
  • For correspondence: duane.froese@ualberta.ca beth.shapiro@gmail.com
Mathias Stiller
bDepartment of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;
cGerman Cancer Consortium, German Cancer Research Center, Institute for Translational Skin Cancer Research, D-45141 Essen, Germany;
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Peter D. Heintzman
bDepartment of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;
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  • ORCID record for Peter D. Heintzman
Alberto V. Reyes
aDepartment of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, Canada T6G 2E3;
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  • ORCID record for Alberto V. Reyes
Grant D. Zazula
dYukon Palaeontology Program, Department of Tourism & Culture, Government of Yukon, Whitehorse, YT, Canada Y1A 2C6;
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André E. R. Soares
bDepartment of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;
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  • ORCID record for André E. R. Soares
Matthias Meyer
eDepartment of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany;
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Elizabeth Hall
dYukon Palaeontology Program, Department of Tourism & Culture, Government of Yukon, Whitehorse, YT, Canada Y1A 2C6;
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Britta J. L. Jensen
aDepartment of Earth and Atmospheric Sciences, University of Alberta, Edmonton, AB, Canada T6G 2E3;
fRoyal Alberta Museum, Edmonton, AB, Canada T5N 0M6;
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Lee J. Arnold
gSchool of Physical Sciences, Environment Institute, and Institute for Photonics and Advanced Sensing, University of Adelaide, Adelaide, SA 5005, Australia;
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Ross D. E. MacPhee
hDivision of Vertebrate Zoology, American Museum of Natural History, New York, NY 10024;
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  • ORCID record for Ross D. E. MacPhee
Beth Shapiro
bDepartment of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA 95064;
iUniversity of California, Santa Cruz Genomics Institute, University of California, Santa Cruz, CA 95064
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  • For correspondence: duane.froese@ualberta.ca beth.shapiro@gmail.com
  1. Edited by Donald K. Grayson, University of Washington, Seattle, WA, and approved February 3, 2017 (received for review December 20, 2016)

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Significance

The appearance of bison in North America is both ecologically and paleontologically significant. We analyzed mitochondrial DNA from the oldest known North American bison fossils to reveal that bison were present in northern North America by 195–135 thousand y ago, having entered from Asia via the Bering Land Bridge. After their arrival, bison quickly colonized much of the rest of the continent, where they rapidly diversified phenotypically, producing, for example, the giant long-horned morphotype Bison latifrons during the last interglaciation.

Abstract

The arrival of bison in North America marks one of the most successful large-mammal dispersals from Asia within the last million years, yet the timing and nature of this event remain poorly determined. Here, we used a combined paleontological and paleogenomic approach to provide a robust timeline for the entry and subsequent evolution of bison within North America. We characterized two fossil-rich localities in Canada’s Yukon and identified the oldest well-constrained bison fossil in North America, a 130,000-y-old steppe bison, Bison cf. priscus. We extracted and sequenced mitochondrial genomes from both this bison and from the remains of a recently discovered, ∼120,000-y-old giant long-horned bison, Bison latifrons, from Snowmass, Colorado. We analyzed these and 44 other bison mitogenomes with ages that span the Late Pleistocene, and identified two waves of bison dispersal into North America from Asia, the earliest of which occurred ∼195–135 thousand y ago and preceded the morphological diversification of North American bison, and the second of which occurred during the Late Pleistocene, ∼45–21 thousand y ago. This chronological arc establishes that bison first entered North America during the sea level lowstand accompanying marine isotope stage 6, rejecting earlier records of bison in North America. After their invasion, bison rapidly colonized North America during the last interglaciation, spreading from Alaska through continental North America; they have been continuously resident since then.

  • Beringia
  • Bison latifrons
  • Bison priscus
  • paleogenomics
  • Rancholabrean
  • steppe bison

Footnotes

  • ↵1To whom correspondence may be addressed. Email: duane.froese{at}ualberta.ca or beth.shapiro{at}gmail.com.
  • Author contributions: D.F. and B.S. designed research; D.F., M.S., P.D.H., A.V.R., G.D.Z., A.E.R.S., M.M., E.H., B.J.L.J., L.J.A., R.D.E.M., and B.S. performed research; G.D.Z. and L.J.A. contributed new reagents/analytic tools; P.D.H., A.V.R., A.E.R.S., and L.J.A. analyzed data; and D.F., P.D.H., A.V.R., G.D.Z., M.M., L.J.A., R.D.E.M., and B.S. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KX269109, and KX269112–KX269145).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1620754114/-/DCSupplemental.

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Timing of bison arrival in North America
Duane Froese, Mathias Stiller, Peter D. Heintzman, Alberto V. Reyes, Grant D. Zazula, André E. R. Soares, Matthias Meyer, Elizabeth Hall, Britta J. L. Jensen, Lee J. Arnold, Ross D. E. MacPhee, Beth Shapiro
Proceedings of the National Academy of Sciences Mar 2017, 114 (13) 3457-3462; DOI: 10.1073/pnas.1620754114

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Timing of bison arrival in North America
Duane Froese, Mathias Stiller, Peter D. Heintzman, Alberto V. Reyes, Grant D. Zazula, André E. R. Soares, Matthias Meyer, Elizabeth Hall, Britta J. L. Jensen, Lee J. Arnold, Ross D. E. MacPhee, Beth Shapiro
Proceedings of the National Academy of Sciences Mar 2017, 114 (13) 3457-3462; DOI: 10.1073/pnas.1620754114
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