Clade II was much more geographically widespread during MIS 3 than it is today and comprised brown bears from Siberia, Alaska, and modern-day Britain and Ireland, as well as the two ancient polar bear matrilines ( Figure 1 ). After the last glacial maximum (LGM), clade II was isolated to small regions of Alaska (ABC islands) and the vicinity of modern-day Ireland ( Figure 1 ). Modern brown bears living on the ABC islands share a matrilineal common ancestor 37–10 kya (median 24 kya), a timing coincident with climatic changes surrounding the LGM that may have led to their isolation from brown bears living on the mainland. In Ireland, brown bears carrying the clade II matriline are present prior to 26 kya and again after 12 kya, but no bear fossils of any kind have been dated to the LGM ( Table S2 Figure 3 ), suggesting that suitable habitat may not have persisted in Ireland through the peak of the last ice age.

Locations of origin (A) and uncalibrated accelerator mass spectrometry radiocarbon ages and mtDNA clade assignments (B) for British and Irish bears included in study. The shaded area in (A) indicates the traditional limit of the last glacial maximum (LGM) in Ireland. However, recent work suggests that the shaded area probably represents a subsequent ice sheet readvance occurring 20.9–14.7 kya [] and that Ireland was completely covered in ice from circa 27–23 kya []. Details of the Irish bear samples and ancient DNA sequencing are provided in Table S2

The recent history of polar bear and brown bear matrilines was characterized by long periods of geographic stability punctuated by episodes of rapid matrilineal dispersal, often over considerable geographic distances ( Figure 1 Figure 2 ; see also Figure S1 available online). This is best illustrated by the inferred radiation of brown bears out of Alaska during the marine isotope stage (MIS) 3 interstadial (Bayes factor, BF [], support for Alaska in comparison to any other location = 45), which was a period of peak environmental conditions for ice-age megafauna []. This rapid, long-distance radiation (clade IIIa, Figure 1 ) established clusters of closely related matrilines in Japan, Kamchatka, Siberia, and both Eastern and Central Europe by 14 kya.

Map indicating the 13 locations to which each matriline was assigned and the 14 significant diffusion pathways that describe the maternal phylogeographic history of brown bears and polar bears over the last circa 120 kya. For the phylogeographic analyses, we assigned all polar bears to a single geographic location, depicted here as Svalbard. Nonreversible diffusion rates are estimated across the entire distribution of posterior trees and therefore reflect average rates of diffusion over time. Rates are considered to be significantly different from zero with Bayes factor (BF) > 8. The significant diffusion pathways are shown in pink, with increasing significance indicated by darker shades and arrows indicating the direction of diffusion. An interactive visualization of the diffusion process of the ancestral bear matrilines over time is available at http://www.phylogeography.org/BEARS.html Figure S2 describes the results of two sensitivity analyses performed to assess the phylogeographic results depicted here and in Figure 1

Maximum clade credibility (MCC) genealogy resulting from a phylogeographic BEAST [] analysis of 242 brown bears and polar bears ranging in age from 120 thousand years ago (kya) to modern. Colors along the branches describe the most probable geographic location of each lineage. Black circles indicate major nodes with >85% posterior support, summarized from the combined output of three Markov chain Monte Carlo chains run for 150 million iterations each and sampled every 10,000 iterations. Letters A–C highlight nodes discussed in the main text. Background shades of gray indicate warm (light gray) and cool (dark gray) marine isotope stages. As noted previously [], the branching order among the earliest diverging branches is not well resolved, with the exception of very high support (99.97%) for monophyly of the clade III/IV lineage. See also Figure S1 Table S1 contains detailed information about the specimens used in this analysis.

The Origin and Evolution of the Polar Bear Matriline

As has been shown previously, all modern polar bear matrilines cluster within clade II ( Figure 1 ). However, in contrast to previous analyses, we found no evidence for reciprocal monophyly between brown and polar bears within this clade, nor do our results support a sister relationship of polar bears with the ABC island brown bears. Instead, the inferred common matrilineal ancestor of modern polar bears falls within the genetic diversity of Irish brown bears (BF = 53). The low posterior support for modern polar bear monophyly ( Figure 1 , node A) is due to modern polar bear lineages frequently clustering into several clades within the diversity of clade II Irish brown bears in the posterior distribution of trees.

10 Lindqvist C.

Schuster S.C.

Sun Y.

Talbot S.L.

Qi J.

Ratan A.

Tomsho L.P.

Kasson L.

Zeyl E.

Aars J.

et al. Complete mitochondrial genome of a Pleistocene jawbone unveils the origin of polar bear. 20 Ingólfsson Ó.

Wiig Ø. Late Pleistocene fossil find in Svalbard: The oldest remains of a polar bear (Ursus maritimus Phipps, 1744) ever discovered. 14 Davison J.

Ho S.Y.W.

Bray S.

Korsten M.

Vulla E.

Hindrikson M.

Østbye K.

Østbye E.

Lauritzen S.-E.

Austin J.

et al. Late-Quaternary biogeographic scenarios for a wild mammal model species, the brown bear (Ursus arctos). 14 Davison J.

Ho S.Y.W.

Bray S.

Korsten M.

Vulla E.

Hindrikson M.

Østbye K.

Østbye E.

Lauritzen S.-E.

Austin J.

et al. Late-Quaternary biogeographic scenarios for a wild mammal model species, the brown bear (Ursus arctos). The two older polar bear matrilines, one isolated from a jawbone from Svalbard [] associated with a stratigraphic layer dated to 130–110 kya [] and another from a rib bone from northern Norway believed to date to circa 115 kya [], also fall within clade II ( Figure 1 , node B). However, although these two sequences are closely related to each other, they are not directly ancestral to the modern polar bear matriline: modern polar bear matrilines cluster with the ancient polar bear matrilines with less than 5% posterior probability. If incomplete lineage sorting were to explain these results, as suggested previously [], the coalescent event of the two lineages in question would have to have taken place prior to speciation. Because the coalescence of all modern polar bear matrilines postdates the age of the two ancient bears (and therefore the speciation date), hybridization followed by matrilineal introgression is much more likely than incomplete lineage sorting to explain the observed data.

Figure 4 Three Hypothetical Scenarios Describing the Divergence between Brown Bear and Polar Bear Matrilines Show full caption (A) Recent speciation. (B) Medium speciation plus multiple hybridization events. (C) Ancient speciation plus more recent hybridization. The branching order of the bear matrilines is based on the MCC tree in Figure 1 . Colored background shading indicates the hypothetical polar bear (blue) and brown bear (yellow) autosomal lineages. Figure 4 describes three hypothetical scenarios that may explain the phylogeographic relationships presented here. In the scenario depicted in Figure 4 A, the timing of the initial divergence between brown bear and polar bear matrilines is the same as our estimated MRCA of modern polar bear matrilines. This scenario describes most closely the prevailing hypothesis explaining the mitochondrial data: a sister relationship between polar bear matrilines and those of ABC island brown bears. However, although it is consistent with conditions during the LGM favoring the emergence of a cold-adapted species, the timeline of this scenario conflicts with both the existence of the two ancient polar bears and the high degree of morphological and behavioral dissimilarity between brown bears and polar bears. This hypothesis could only be tenable if the ancient polar bear sequences contain errors that force them to fall erroneously outside of the diversity of the modern polar bears and the ancient Irish and ABC island brown bears.

21 Shapiro B.

Ho S.Y.

Drummond A.J.

Suchard M.A.

Pybus O.G.

Rambaut A. A Bayesian phylogenetic method to estimate unknown sequence ages. 10 Lindqvist C.

Schuster S.C.

Sun Y.

Talbot S.L.

Qi J.

Ratan A.

Tomsho L.P.

Kasson L.

Zeyl E.

Aars J.

et al. Complete mitochondrial genome of a Pleistocene jawbone unveils the origin of polar bear. 14 Davison J.

Ho S.Y.W.

Bray S.

Korsten M.

Vulla E.

Hindrikson M.

Østbye K.

Østbye E.

Lauritzen S.-E.

Austin J.

et al. Late-Quaternary biogeographic scenarios for a wild mammal model species, the brown bear (Ursus arctos). 14 Davison J.

Ho S.Y.W.

Bray S.

Korsten M.

Vulla E.

Hindrikson M.

Østbye K.

Østbye E.

Lauritzen S.-E.

Austin J.

et al. Late-Quaternary biogeographic scenarios for a wild mammal model species, the brown bear (Ursus arctos). The scenario depicted in Figure 4 B accommodates the two ancient polar bears by allowing brown bear and polar bear matrilines to diverge earlier than depicted in Figure 4 A. In this scenario, the maternal MRCA of polar bears, Irish brown bears, and ABC island brown bears diverged from ancestral brown bears carrying the clade II matriline during the Pleistocene. Because of uncertainty surrounding the age of the two ancient polar bear fossils, we allow the age of both mitochondrial lineages to be random variables drawn from a distribution ranging from the oldest bound on their stratigraphic dates (130 kya) to the most recent bound on their radiocarbon dates (40 kya) using a tip-sampling method []. The estimated age of the MRCA of clade II matrilines is 135–111 kya, roughly similar to but slightly younger than that estimated by either Lindqvist et al. [] (152 kya) or Davison et al. [] (160 kya). This most likely reflects differences between methods used to calibrate the molecular clock, because the incorporation of an external (fossil) calibration will result in a slower overall evolutionary rate []. In our analyses, the age of this particular node is highly influenced by the age of the ancient polar bears. When the ages of the two ancient polar bear sequences are sampled between 130–100 kya, rather than 130–40 kya, the estimated age of the MRCA of this node is 166–120 kya, overlapping with both our estimates using the less constrained age and the previous estimates.

15 Barnes I.

Matheus P.

Shapiro B.

Jensen D.

Cooper A. Dynamics of Pleistocene population extinctions in Beringian brown bears. If the Irish bears carrying clade II matrilines, or at least those Irish bears associated with radiocarbon ages postdating the LGM, were actually polar bears and not brown bears, then fewer hybridization events would be required to explain the observed data (in Figure 4 B, only the transfer of the polar bear matriline to the ABC island brown bears would be required). However, bone isotopic data indicates that all Irish bears had a terrestrial diet similar to that of late Pleistocene brown bears from Alaska [] and dissimilar to the markedly marine diet of polar bears ( Supplemental Experimental Procedures ). The scenario depicted in Figure 4 B therefore predicts the following: an older polar bear matriline, represented in our analysis by the two ancient polar bears, became widespread across the Arctic. These polar bears hybridized opportunistically with small, coastal populations of brown bears, leading in at least two instances to fixation of the polar bear matriline in brown bear populations (Ireland and the ABC islands). More recently, additional hybridization occurred in Ireland, followed by fixation of the Irish brown bear matriline in polar bears. This marks the MRCA of the modern polar bear matriline.

15 Barnes I.

Matheus P.

Shapiro B.

Jensen D.

Cooper A. Dynamics of Pleistocene population extinctions in Beringian brown bears. 15 Barnes I.

Matheus P.

Shapiro B.

Jensen D.

Cooper A. Dynamics of Pleistocene population extinctions in Beringian brown bears. A single bear from Fairbanks, Alaska whose mtDNA sequence was isolated as part of a previous study [] also falls within the cluster of Irish brown bear and modern polar bear matrilines. The fossil from which this sequence was isolated is part of a large, geographically extensive collection of bones from across Alaska made by Otto Geist in the late 1930s that is now housed at the American Museum of Natural History in New York. Because the fossil was an ulna belonging to a juvenile, it could only be identified morphologically as Ursus. However, unlike the Irish brown bears, the isotopic signature of this Alaskan bear is decidedly marine [], leading the authors of the original publication to conclude that the specimen was incorrectly provenanced and likely came from the coast of Alaska rather than from Fairbanks. Even if the provenance of this specimen is wrong, its radiocarbon age (19,360 ± 140 uncalibrated radiocarbon years before present; lab accession number OxA-10036) suggests that polar bears with clade II matrilines were present in Alaska throughout the LGM, providing additional support for the multiple-hybridization scenario depicted in Figure 4 B and making it possible that more than one Irish matriline was captured by polar bears prior to the Holarctic fixation of the modern matriline.

5 Kurtén B. The evolution of the polar bear, Ursus maritimus (Phipps). 7 Pagès M.

Calvignac S.

Klein C.

Paris M.

Hughes S.

Hänni C. Combined analysis of fourteen nuclear genes refines the Ursidae phylogeny. 8 Yu L.

Li Q.W.

Ryder O.A.

Zhang Y.P. Phylogeny of the bears (Ursidae) based on nuclear and mitochondrial genes. 22 Nakagome S.

Pecon-Slattery J.

Masuda R. Unequal rates of Y chromosome gene divergence during speciation of the family Ursidae. In Figure 4 C, brown bear and polar bear matrilines diverged prior to the mitochondrial diversification within brown bears. This allows more time for the evolution of each species' distinctive phenotype and is consistent with hypotheses of at least a Middle Pleistocene origin for polar bears [] but requires multiple hybridizations with brown bears to explain both the Svalbard polar bear matriline and the modern polar bear matriline. If this hypothesis is correct, autosomal markers should support a divergence between polar bears and brown bears prior to the divergence of all extant brown bears. To test this, we analyzed 20 nuclear loci isolated from all eight extant species within the Ursidae []. The small evolutionary distance between brown bears and polar bears prohibits precise estimates of the brown/polar divergence; however, the 95% highest posterior density interval of estimated coalescence dates spans the interval 2 Mya–400 kya. Although there are a number of reasons unrelated to hybridization why the mitochondrial MRCA would be more recent than most autosomal common ancestor dates, such as a smaller mitochondrial effective population size, this date range predates by a considerable margin the estimated MRCA of polar bear and brown bear matrilines.

e ): if the mitochondrial haplotypes were selectively equivalent and assuming a female N e of 2,025 based on an estimated 18% of females reproducing in a total census size of 10,000–12,500 females and a female generation time of 9.7 years [ 23 Cronin M.A.

Amstrup S.C.

Talbot S.L.

Sage G.K.

Amstrup K.S. Genetic variation, relatedness, and effective population size of polar bears (Ursus maritimus) in the southern Beaufort Sea, Alaska. Regardless of which scenario prevails, modern polar bears across their Holarctic distribution all share a common matrilineal ancestor within the last 51–20 kya. If polar bears were already widely distributed at this time, this suggests a complete replacement of the previous mitochondrial lineage within a remarkably short time frame. Such a recent coalescence is feasible given current estimates of their effective population size (N): if the mitochondrial haplotypes were selectively equivalent and assuming a female Nof 2,025 based on an estimated 18% of females reproducing in a total census size of 10,000–12,500 females and a female generation time of 9.7 years [], our sample of 51 modern mitochondrial alleles would coalesce with 95% probability in 93.2–12.9 kya (median 33.4 kya; Supplemental Experimental Procedures ).