Fossil and genomic evidence constrains the timing of bison arrival in North America
Edited by Donald K. Grayson, University of Washington, Seattle, WA, and approved February 3, 2017 (received for review December 20, 2016)
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.
Data Availability
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KX269109, and KX269112–KX269145).
Acknowledgments
We thank Andrew Fields, Brandon Letts, Dan Chang, Joshua Kapp, and Amanda Hart for technical assistance; Ben J. Novak for the bison skull paintings in Fig. 2; Ian Miller, Joe Sertich, and the Denver Museum of Nature and Science for access to the Snowmass sample; and Harold Frost, Jr. and the late Stephen Charlie for assistance in the field. Access and support to work at the Old Crow sites was facilitated by the Heritage Department of the Vuntut Gwitchin Government. This work used the Vincent J. Coates Genomics Sequencing Laboratory at University of California, Berkeley, supported by NIH S10 Instrumentation Grants S10RR029668 and S10RR027303. Support was provided from Yukon Heritage Branch; Natural Resources Canada Polar Continental Shelf Program (D.F.), Canada Research Chairs program, and Natural Sciences and Engineering Research Council (D.F.); National Science Foundation ARC-09090456 and ARC-1417046, and Gordon and Betty Moore Foundation GBMF3804 (to B.S.); and Australian Research Council DP0878604 and FT130100195 (to L.J.A.).
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References
1
AK Knapp, et al., The keystone role of bison in North American tallgrass prairie. Bioscience 49, 39–50 (1999).
2
RD Guthrie, Bison evolution and zoogeography in North America during the Pleistocene. Q Rev Biol 45, 1–15 (1970).
3
B Shapiro, et al., Rise and fall of the Beringian steppe bison. Science 306, 1561–1565 (2004).
4
GC Frison Prehistoric Hunters of the High Plains (Academic, New York, 1978).
5
CH Freese, et al., Second chance for the plains bison. Biol Conserv 136, 175–184 (2007).
6
BJ MacFadden, Horses, the fossil record, and evolution. Evolutionary Biology, eds MK Hecht, B Wallace, GT Prance (Springer, New York) Vol 22, 131–158 (1988).
7
AM Lister, AV Sher, Evolution and dispersal of mammoths across the Northern Hemisphere. Science 350, 805–809 (2015).
8
CJ Bell, et al., The North American Pliocene and Pleistocene sequences. Cenozoic Mammals of North America, ed MO Woodburne (Univ of California Press, Berkeley, 2004).
9
DE Savage, Late Cenozoic vertebrates of the San Francisco Bay region, California. Publ Depart Geol Sci 28, 1–30 (1951).
10
AD Barnosky, et al., Prelude to the Anthropocene: Two new North American land mammal ages (NALMAs). Anthropol Rev 1, 225–242 (2014).
11
JN McDonald, GS Morgan, The appearance of bison in North America. Curr Res Pleist 16, 127–129 (1999).
12
TL Péwé, Quaternary Geology of Alaska, USGS Professional Paper 835 (US Government Print Office, Washington, DC), Vol 835. (1975).
13
TD Hamilton, JL Craig, PV Sellman, The Fox permafrost tunnel: A Late Quaternary geologic record in central Alaska. GSA Bull 100, 948–969 (1988).
14
SJ Preece, JA Westgate, BA Stemper, TL Pewe, Tephrochronology of late Cenozoic loess at Fairbanks, central Alaska. GSA Bull 111, 71–90 (1999).
15
AE Sanders, RE Weems, III LB Albright, Formalization of the Middle Pleistocene ‘Ten Mile Hill Beds’ in South Carolina with evidence for placement of the Irvingtonian-Rancholabrean boundary. Papers on Geology, Vertebrate Paleontology, and Biostratigraphy in Honor of Michael O. Woodburne, ed Albright, III LB (Museum of Northern Arizizona, Flagstaff, AZ), Vol 65, pp 363–370. (2009).
16
BJ Szabo, Uranium-series dating of fossil corals from marine sediments of southeastern United States Atlantic Coastal Plain. GSA Bull 96, 398–406 (1985).
17
JT Hollin, PJ Hearty, South Carolina interglacial sites and stage 5 sea levels. Quat Res 33, 1–17 (1990).
18
CJ Bell, CA Repenning, Observations on dental variation in Microtus from the Cudahy Ash Pit Fauna, Meade County, Kansas and implications for Irvingtonian microtine rodent biochronology. J Vert Paleont 19, 757–766 (1999).
19
CB Schultz, LD Martin, Biostratigraphy of the Neogene-Quaternary boundary in North America. Proceedings of the 2nd Symposium of the Neogene-Quaternary Boundary, Bologna. G Geol XLI, 285–295 (1977).
20
SL Forman, J Pierson, Late Pleistocene luminescence chronology of loess deposition in the Missouri and Mississippi river valleys, United States. Paleo3 186, 25–46 (2002).
21
L Orlando, et al., Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 499, 74–78 (2013).
22
JE Storer, A Middle Pleistocene (late Irvingtonian) Mammalian fauna from Thistle Creek, Klondike Goldfields Region of Yukon Territory, Canada. Paludicola 4, 115–155 (2004).
23
JA Westgate, et al., Changing ideas on the identity and stratigraphic significance of the Sheep Creek tephra beds in Alaska and the Yukon Territory, northwestern North America. Quat Int 178, 183–209 (2008).
24
IM Miller, et al., Summary of the Snowmastodon Project Special Volume: A high-elevation, multi-proxy biotic and environmental record of MIS 6–4 from the Ziegler Reservoir fossil site, Snowmass Village, Colorado, USA. Quat Res 82, 618–634 (2014).
25
JD Pinsof, The American Falls local fauna: Late Pleistocene (Sangamonian) Vertebrates from Southeastern Idaho. And Whereas...: Papers on the Vertebrate Paleontology of Idaho Honoring John A. White, Volume 1., Occasional Paper 36, eds Akersten WA, McDonald HG, Meldrum DJ, Flint MEJ (Idaho Museum of Natural History, Pocatello, ID.) pp 121–145. (1998).
26
A Drummond, AG Rodrigo, Reconstructing genealogies of serial samples under the assumption of a molecular clock using serial-sample UPGMA. Mol Biol Evol 17, 1807–1815 (2000).
27
AV Jopling, WN Irving, BF Beebe, Stratigraphic, sedimentological and faunal evidence for the occurrence of pre-Sangamonian artefacts in northern Yukon. Arctic 34, 3–33 (1981).
28
S Kuzmina, DG Froese, BJL Jensen, E Hall, GD Zazula, Middle Pleistocene (MIS 7) to Holocene fossil insect assemblages from the Old Crow basin, northern Yukon, Canada. Quat Int 341, 216–242 (2014).
29
S Preece, et al., Old Crow tephra across eastern Beringia: A single cataclysmic eruption at the close of Marine Isotope Stage 6. Quat Sci Rev 30, 2069–2090 (2011).
30
AV Reyes, DG Froese, BJL Jensen, Permafrost response to last interglacial warming: Field evidence from non-glaciated Yukon and Alaska. Quat Sci Rev 29, 3256–3274 (2010).
31
Jr JV Matthews, CE Schweger, JA Janssens, The last (Koy-Yukon) interglaciation in the northern Yukon: Evidence from Unit 4 at Ch’ijee’s Bluff, Bluefish Basin. Geogr Phys Quat 44, 341–362 (1990).
32
B Shapiro, M Hofreiter, A paleogenomic perspective on evolution and gene function: New insights from ancient DNA. Science 343, 1236573 (2014).
33
KC Douglas, et al., Complete mitochondrial DNA sequence analysis of Bison bison and bison-cattle hybrids: Function and phylogeny. Mitochondrion 11, 166–175 (2011).
34
A Achilli, et al., Mitochondrial genomes of extinct aurochs survive in domestic cattle. Curr Biol 18, R157–R158 (2008).
35
IV Kirillova, et al., An ancient bison from the mouth of the Rauchua River (Chukotka, Russia). Quat Res 84, 232–245 (2015).
36
A Hu, et al., Influence of Bering Strait flow and North Atlantic circulation on glacial sea-level changes. Nat Geosci 3, 118–121 (2010).
37
C Waelbroeck, et al., Sea-level and deep water temperature changes derived from benthic foraminifera isotopic records. Quat Sci Rev 21, 295–305 (2002).
38
AV Reyes, et al., A late–Middle Pleistocene (Marine Isotope Stage 6) vegetated surface buried by Old Crow tephra at the Palisades, interior Alaska. Quat Sci Rev 29, 801–811 (2010).
39
MJ Aitken An Introduction to Optical Dating: The Dating of Quaternary Sediments by the Use of Photon-Stimulated Luminescence (Oxford Univ Press, Oxford, 1998).
40
LJ Arnold, M Demuro, M Navazo Ruiz, A Benito-Calvo, A Pérez-González, OSL dating of the Middle Palaeolithic Hotel California site, Sierra de Atapuerca, north-central Spain. Boreas 42, 285–305 (2013).
41
LJ Arnold, M Demuro, M Navazo Ruiz, Empirical insights into multi-grain averaging effects from ‘pseudo’ single-grain OSL measurements. Radiat Meas 47, 652–658 (2012).
42
LJ Arnold, RG Roberts, Stochastic modelling of multi-grain equivalent dose (De) distributions: Implications for OSL dating of sediment mixtures. Quat Geochronol 4, 204–230 (2009).
43
RF Galbraith, RG Roberts, GM Laslett, H Yoshida, JM Olley, Optical dating of single and multiple grains of quartz from Jinmium rock shelter, northern Australia: Part I, experimental design and statistical models. Archaeometry 41, 339–364 (1999).
44
J Dabney, et al., Complete mitochondrial genome sequence of a Middle Pleistocene cave bear reconstructed from ultrashort DNA fragments. Proc Natl Acad Sci USA 110, 15758–15763 (2013).
45
N Rohland, H Siedel, M Hofreiter, A rapid column-based ancient DNA extraction method for increased sample throughput. Mol Ecol Resour 10, 677–683 (2010).
46
M Meyer, M Kircher, Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harbor Protoc 2010, pdb.prot5448 (2010).
47
MT Gansauge, M Meyer, Single-stranded DNA library preparation for the sequencing of ancient or damaged DNA. Nat Protoc 8, 737–748 (2013).
48
V Slon, et al., Mammalian mitochondrial capture, a tool for rapid screening of DNA preservation in faunal and undiagnostic remains, and its application to Middle Pleistocene specimens from Qesem Cave (Israel). Quat Int 398, 210–218 (2016).
49
H Li, R Durbin, Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
50
AW Briggs, et al., Targeted retrieval and analysis of five Neandertal mtDNA genomes. Science 325, 318–321 (2009).
51
M Meyer, et al., A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505, 403–406 (2014).
52
H Jónsson, A Ginolhac, M Schubert, PL Johnson, L Orlando, mapDamage2.0: Fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29, 1682–1684 (2013).
53
R Lanfear, B Calcott, SYW Ho, S Guindon, Partitionfinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29, 1695–1701 (2012).
54
AJ Drummond, MA Suchard, D Xie, A Rambaut, Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29, 1969–1973 (2012).
55
MS Gill, et al., Improving Bayesian population dynamics inference: A coalescent-based model for multiple loci. Mol Biol Evol 30, 713–724 (2013).
56
B Shapiro, et al., A Bayesian phylogenetic method to estimate unknown sequence ages. Mol Biol Evol 28, 879–887 (2011).
57
RD Guthrie Frozen Fauna of the Mammoth Steppe (Univ of Chicago Press, Chicago, IL, 1990).
58
MF Skinner, OC Kaisen, The fossil bison of Alaska and preliminary revision of the genus. Bull Am Mus Nat Hist 89, 123–256 (1947).
59
GW Berger, Luminescence chronology of late Pleistocene loess-paleosol and tephra sequences near Fairbanks, Alaska. Quat Res 60, 70–83 (2003).
60
M Auclair, M Lamothe, F Lagroix, SK Banerjee, Luminescence investigation of loess and tephra from Halfway House section, Central Alaska. Quat Geochronol 2, 34–38 (2007).
61
TL Péwé, GW Berger, JA Westgate, PM Brown, SW Leavitt, Eva Interglaciation Forest Bed, unglaciated east-central Alaska: Global warming 125,000 years ago. GSA Special Publication. (1997).
62
TD Hamilton, J Brigham-Grette, The last interglaciation in Alaska: Stratigraphy and paleoecology of potential sites. Quat Int 10-12, 49–71 (1991).
63
P Matheus, J Begét, O Mason, C Gelvin-Reymiller, Late Pliocene to late Pleistocene environments preserved at the Palisades Site, central Yukon River, Alaska. Quat Res 60, 33–43 (2003).
64
PF McDowell, ME Edwards, Evidence of Quaternary climatic variations in a sequence of loess and related deposits at Birch Creek, Alaska: Implications for the stage 5 climatic chronology. Quat Sci Rev 20, 63–76 (2001).
65
OL Hughes, et al., Upper Pleistocene stratigraphy, paleoecology and archeology of northern Yukon interior, eastern Beringia 1. Bonnet Plume Basin. Arctic 34, 329–365 (1981).
66
CR Harington, Pleistocene vertebrates of the Yukon Territory. Quat Sci Rev 30, 2341–2354 (2011).
67
CE Schweger, The Old Crow and Bluefish basin, Northern Yukon: development of the Quaternary history. Late Cenozoic History of the Interior Basins of Alaska and the Yukon, eds Carter DL, Hamilton TD, Galloway, JP (US Geological Survey, Washington, DC) pp 30–33. (1989).
68
KE Kennedy, DG Froese, GD Zazula, B Lauriol, Last Glacial Maximum age for the northwest Laurentide maximum from the Eagle River spillway and delta complex, northern Yukon. Quat Sci Rev 29, 1288–1300 (2010).
69
GD Zazula, A Duk-Rodkin, CE Schweger, RE Morlan, Late Pleistocene chronology of glacial Lake Old Crow and the north-west margin of the Laurentide Ice Sheet. Quaternary Glaciations - Extent and Chronology, Part II. (Elsevier, Amsterdam) pp 347–362. (2004).
70
AS Murray, AG Wintle, Luminescence dating of quartz using an improved single-aliquot regenerative-dose procedure. Radiat Meas 32, 57–73 (2000).
71
LJ Arnold, et al., Paper II—Dirt, dates and DNA: OSL and radiocarbon chronologies of perennially frozen sediments in Siberia, and their implications for sedimentary ancient DNA studies. Boreas 40, 417–445 (2011).
72
Z Jacobs, GAT Duller, AG Wintle, Interpretation of single-grain De distributions and calculation of De. Radiat Meas 41, 264–277 (2006).
73
H Yoshida, RG Roberts, JM Olley, GM Laslett, RF Galbraith, Extending the age range of optical dating using single ‘supergrains’ of quartz. Radiat Meas 32, 439–446 (2000).
74
AG Wintle, AS Murray, A review of quartz optically stimulated luminescence characteristics and their relevance in single-aliquot regeneration dating protocols. Radiat Meas 41, 369–391 (2006).
75
LJ Arnold, RG Roberts, Paper I—Optically stimulated luminescence (OSL) dating of perennially frozen deposits in north-central Siberia: OSL characteristics of quartz grains and methodological considerations regarding their suitability for dating. Boreas 40, 389–416 (2011).
76
LJ Arnold, RG Roberts, RF Galbraith, SB DeLong, A revised burial dose estimation procedure for optical dating of young and modern-age sediments. Quat Geochronol 4, 306–325 (2009).
77
RF Galbraith, PF Green, Estimating the component ages in a finite mixture. Nucl Tracks Radiat Meas 17, 197–206 (1990).
78
LE Lisiecki, ME Raymo, A Pliocene-Pleistocene stack of 57 globally distributed benthic δ18O records. Paleoceanography 20, PA1003 (2005).
79
RE Morlan, Paleoecological implications of Late Pleistocene and Holocene microtine rodents from the Bluefish Caves, northern Yukon Territory. Can J Earth Sci 26, 149–156 (1989).
80
CR Harington Annotated Bibliography of Quaternary Vertebrates of Northern North America—With Radiocarbon Dates (Univ of Toronto Press, Toronto), pp. 360 (2003).
81
J Weinstock, et al., Evolution, systematics, and phylogeography of pleistocene horses in the new world: A molecular perspective. PLoS Biol 3, e241 (2005).
82
HG McDonald, CR Harington, G de Iuliis, The ground sloth Megalonyx from Pleistocene deposits of the Old Crow Basin, Yukon, Canada. Arctic 53, 213–220 (2000).
83
J Hoganson, HG McDonald, First report of Jefferson’s ground sloth (Megalonyx jeffersonii) in North Dakota: Paleobiogeographical and paleoecological significance. J Mammal 88, 73–80 (2007).
84
CR Harington, Soergelia: An indicator of Holarctic Middle Pleistocene deposits. Second Annual Muskox Symposium (NRC Canada, Ottawa), pp A1–A9. (1989).
85
OL Hughes, Surficial geology of northern Yukon Territory and northwestern District of Mackenzie, Northwest Territories, Geological Survey of Canada, Paper, (Geological Survey of Canada, Ottawa) Vol 69-36, pp 1–11. (1972).
86
AV Reyes, GD Zazula, S Kuzmina, TA Ager, DG Froese, Identification of last interglacial deposits in eastern Beringia: A cautionary note from the Palisades, interior Alaska. J Quat Sci 26, 345–352 (2011).
87
TL Fulton, Setting up an ancient DNA laboratory. Methods Mol Biol 840, 1–11 (2012).
88
PD Heintzman, et al., Genomic data from extinct North American Camelops revise camel evolutionary history. Mol Biol Evol 32, 2433–2440 (2015).
89
JS Pigati, et al., Geologic setting and stratigraphy of the Ziegler Reservoir fossil site, Snowmass Village, Colorado. Quat Res 82, 477–489 (2014).
90
SA Mahan, et al., A geochronologic framework for the Ziegler Reservoir fossil site, Snowmass Village, Colorado. Quat Res 82, 490–503 (2014).
91
M Kircher, S Sawyer, M Meyer, Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res 40, e3 (2012).
92
T Maricic, M Whitten, S Pääbo, Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS One 5, e14004 (2010).
93
G Renaud, U Stenzel, J Kelso, leeHom: Adaptor trimming and merging for Illumina sequencing reads. Nucleic Acids Res 42, e141 (2014).
94
M Meyer, et al., A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222–226 (2012).
95
J Dabney, M Meyer, S Pääbo, Ancient DNA damage. Cold Spring Harb Perspect Biol 5, 1–7 (2013).
96
AW Briggs, et al., Patterns of damage in genomic DNA sequences from a Neandertal. Proc Natl Acad Sci USA 104, 14616–14621 (2007).
97
ELC Verkaar, IJ Nijman, M Beeke, E Hanekamp, JA Lenstra, Maternal and paternal lineages in cross-breeding bovine species. Has wisent a hybrid origin? Mol Biol Evol 21, 1165–1170 (2004).
98
PD Heintzman, et al., Bison phylogeography constrains dispersal and viability of the Ice Free Corridor in western Canada. Proc Natl Acad Sci USA 113, 8057–8063 (2016).
99
GAT Duller, Distinguishing quartz and feldspar in single grain luminescence measurements. Radiat Meas 37, 161–165 (2003).
100
MJ Aitken Thermoluminescence Dating (Academic, London, 1985).
101
G Adamiec, M Aitken, Dose-rate conversion factors: update. Anc TL 16, 37–50 (1998).
102
S Stokes, et al., Alternative chronologies for Late Quaternary (Last Interglacial–Holocene) deep sea sediments via optical dating of silt-sized quartz. Quat Sci Rev 22, 925–941 (2003).
103
BJ Brennan, Beta doses to spherical grains. Radiat Meas 37, 299–303 (2003).
104
JR Prescott, JT Hutton, Cosmic ray contributions to dose rates for luminescence and ESR dating: Large depths and long-term time variations. Radiat Meas 23, 497–500 (1994).
105
SM Pawley, et al., Age limits on Middle Pleistocene glacial sediments from OSL dating, north Norfolk, UK. Quat Sci Rev 27, 1363–1377 (2008).
106
GAT Duller, Assessing the error on equivalent dose estimates derived from single aliquot regenerative dose measurements. Anc TL 25, 15–24 (2007).
Information & Authors
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Data Availability
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. KX269109, and KX269112–KX269145).
Submission history
Published online: March 13, 2017
Published in issue: March 28, 2017
Keywords
Acknowledgments
We thank Andrew Fields, Brandon Letts, Dan Chang, Joshua Kapp, and Amanda Hart for technical assistance; Ben J. Novak for the bison skull paintings in Fig. 2; Ian Miller, Joe Sertich, and the Denver Museum of Nature and Science for access to the Snowmass sample; and Harold Frost, Jr. and the late Stephen Charlie for assistance in the field. Access and support to work at the Old Crow sites was facilitated by the Heritage Department of the Vuntut Gwitchin Government. This work used the Vincent J. Coates Genomics Sequencing Laboratory at University of California, Berkeley, supported by NIH S10 Instrumentation Grants S10RR029668 and S10RR027303. Support was provided from Yukon Heritage Branch; Natural Resources Canada Polar Continental Shelf Program (D.F.), Canada Research Chairs program, and Natural Sciences and Engineering Research Council (D.F.); National Science Foundation ARC-09090456 and ARC-1417046, and Gordon and Betty Moore Foundation GBMF3804 (to B.S.); and Australian Research Council DP0878604 and FT130100195 (to L.J.A.).
Notes
This article is a PNAS Direct Submission.
Authors
Competing Interests
The authors declare no conflict of interest.
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