Fossil and genomic evidence constrains the timing of bison arrival in North America - PubMed (original) (raw)

. 2017 Mar 28;114(13):3457-3462.

doi: 10.1073/pnas.1620754114. Epub 2017 Mar 13.

Mathias Stiller 2 3, Peter D Heintzman 2, Alberto V Reyes 4, Grant D Zazula 5, André E R Soares 2, Matthias Meyer 6, Elizabeth Hall 5, Britta J L Jensen 4 7, Lee J Arnold 8, Ross D E MacPhee 9, Beth Shapiro 10 11

Affiliations

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

Duane Froese et al. Proc Natl Acad Sci U S A. 2017.

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.

Keywords: Beringia; Bison latifrons; Bison priscus; Rancholabrean; paleogenomics; steppe bison.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

(A) Localities of the 36 fossil bison. Siberia: green; North America north of 60° N: orange; North America south of 60° N: blue. The number of samples is given in italics if >one sample was recovered. The green dashed lines outline the last glacial maximum Bering Land Bridge extent. Insets showing locations of (B) CRH 11 (labeled orange circle) and Ch’ijee’s Bluff (orange star) in northern Yukon, with (C) a zoom-in on Ch’ijee’s Bluff, and (D) Snowmass, Colorado (blue star). (E) Bayesian phylogeny resulting from analysis of the reduced mitochondrial alignment, calibrated using the ages of the bison fossils from which data were generated. Nodes with posterior support of >0.99 are indicated with a black asterisk and other values are provided for deep nodes. The positions of the Ch’ijee’s Bluff and Snowmass bison are highlighted. We identify two waves of dispersal from Asia into North America via the Bering Land Bridge (nodes 1 and 2), with date ranges indicated as light blue bars. Areas of gray shading indicate intervals of lowered sea level sufficient to expose the Bering Land Bridge (36).

Fig. 2.

Fig. 2.

Reconstructions of bison skulls based on fossils attributed to (A) a giant long-horned bison, B. latifrons; (B) a Late Pleistocene steppe bison, B. priscus; and (C) a present-day B. bison. Giant long-horned bison were significantly larger than present-day bison; adult males may have weighed in excess of 2,000 kg, which is twice as large as present-day bison, and had horns that spanned as much as 2.2 m (57, 58).

Fig. 3.

Fig. 3.

Features of the Ch’ijee’s Bluff locality. (A) the Old Crow tephra (124 ± 10 kyBP; UA1206) highlighted by the white arrow, (B) the stratigraphic setting of the Old Crow tephra, bison metacarpal YG 264.1, and the MIS 5e forest bed, and (C) the in situ metacarpal was found several centimeters beneath the prominent MIS 5e forest bed and ∼125 cm above Old Crow tephra (the latter is not shown). The stratigraphy indicates a latest MIS 6 age for YG 264.1.

Fig. S1.

Fig. S1.

Major element geochemistry of Old Crow tephra at CRH 11 and Ch’ijee’s Bluff.

Fig. S2.

Fig. S2.

OSL dose-recovery test results for sample CRH 11-1. (A) Ratios of recovered-to-given dose versus PH1 temperature (held for 10 s) for ∼400-grain aliquots. The natural OSL signals of the multigrain aliquots were optically bleached with two 1-ks blue LED illuminations at ambient temperature, each separated by a 10-ks pause. A known dose of 100 Gy was then administered to each aliquot and the SAR procedure detailed in table S2 of Arnold et al. (41) was subsequently used to estimate this dose. A fixed PH2 of 160 °C for 10 s was applied in the SAR procedure. (B) Radial plot showing ratios of recovered-to-given dose obtained for individual quartz grains using a PH1 of 160 °C for 10 s and a PH2 of 160 °C for 10 s. The single-grain natural OSL signals were bleached using the same procedure outlined above and the administered doses were subsequently recovered using the single-grain SAR procedure shown in Table S1. The gray shaded region on the radial plot is centered on the administered dose for each grain (sample average = 315 Gy; although this amount varied from 265 to 353 Gy for individual grains, because of spatial variations in the dose rate of the β source). Individual De values that fall within the shaded region are consistent with the administered dose at 2σ.

Fig. S3.

Fig. S3.

Representative OSL decay and dose–response curves for individual quartz grains from the CRH 11 samples. Sensitivity-corrected dose–response curves were constructed using the first 0.17 s of each green laser stimulation after subtracting a mean background count obtained from the last 0.25 s of the OSL signal. (A) Quartz grain from CRH 11-2 with a relatively bright OSL signal (_T_n >500 counts/0.17 s). (B) Quartz grain from sample CRH 11-3 with an average OSL signal (_T_n = ∼200–300 counts/0.17 s). (C) Quartz grain from CRH 11-2 with a particularly high characteristic saturation dose (D0) value of >350 Gy. In the inset plots, the open circles on the y axis denote the sensitivity-corrected natural OSL signals, and the sensitivity-corrected regenerated OSL signals are shown as filled circles.

Fig. S4.

Fig. S4.

Single-grain De distributions for the four CRH 11 OSL samples, shown as radial plots (A–D). The De value for each grain is read by drawing a line from the origin of the y axis (Standardized Estimate), through the data point of interest, to the radial axis (plotted on a log scale) on the right-hand side; the point of intersection is the De (in Gy). The measurement error on this De is obtained by extending a line vertically to the x axis, where the point of intersection is the relative SE (shown as a percentage of the De value) and its reciprocal (Precision). In radial plots, the most precise estimates fall furthest to the right, and the least precise estimates fall furthest to the left. Here, the gray bands are centered on the weighted mean De values used to calculate the OSL ages, which we estimated using the CAM of Galbraith et al. (43).

Fig. S5.

Fig. S5.

Maximum clade credibility trees resulting from the Bayesian analysis of the reduced (A) and full (B) mitochondrial genome data sets. The reduced dataset (A) is also depicted in Fig. 1_E_. Colors are as in Fig. 1. Numbers along the branches are Bayesian posterior probability scores for each clade. Bars represent 95% highest posterior probability density intervals for node heights and are reported for nodes with a posterior probability score of >0.95 (A) or >0.85 (B). Tip labels follow the convention of sampleID_locality/species_age as in Dataset S1.

Fig. S6.

Fig. S6.

DNA damage patterns for the Ch’ijee’s Bluff steppe bison (MS226/DC009) (A–C), B. latifrons from Snowmass (B5493) (D–F), two Siberian steppe bison (AE006, G–I) (AE010, J–L), and two steppe bison from North America (PH027, M–O) (MS220, P–R). Damage patterns include DNA fragment length distributions (A, D, G, J, M, P), fragmentation patterns (B, E, H, K, N, Q), and misincorporation rates (C, F, I, L, O, R), the latter of which are cytosine to thymine (red lines) and guanine to adenine (blue lines) misincorporations. PH027 was previously reported in Heintzman et al. (98).

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