Ancient hybridization and an Irish origin for the modern polar bear matriline

Abstract

Background: Polar bears (Ursus maritimus) are among those species most susceptible to the rapidly changing arctic climate, and their survival is of global concern. Despite this, little is known about polar bear species history. Future conservation strategies would significantly benefit from an understanding of basic evolutionary information, such as the timing and conditions of their initial divergence from brown bears (U. arctos) or their response to previous environmental change.

Results: We used a spatially explicit phylogeographic model to estimate the dynamics of 242 brown bear and polar bear matrilines sampled throughout the last 120,000 years and across their present and past geographic ranges. Our results show that the present distribution of these matrilines was shaped by a combination of regional stability and rapid, long-distance dispersal from ice-age refugia. In addition, hybridization between polar bears and brown bears may have occurred multiple times throughout the Late Pleistocene.

Conclusions: The reconstructed matrilineal history of brown and polar bears has two striking features. First, it is punctuated by dramatic and discrete climate-driven dispersal events. Second, opportunistic mating between these two species as their ranges overlapped has left a strong genetic imprint. In particular, a likely genetic exchange with extinct Irish brown bears forms the origin of the modern polar bear matriline. This suggests that interspecific hybridization not only may be more common than previously considered but may be a mechanism by which species deal with marginal habitats during periods of environmental deterioration.

Figure 1. Maximum Clade Credibility Genealogy Describing the Estimated Evolutionary History of Sampled Brown and Polar Bear Matrilines

Maximum clade credibility (MCC) genealogy resulting from a phylogeographic BEAST [39] 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 [15, 16], 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.

Figure 2. Reconstructed Spatial Diffusion Pathways of Brown and Polar Bear Matrilines over the Last 120,000 Years

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.

Figure 3. Ages and Geographic Locations of the Sampled Fossil British and Irish Brown Bears

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 [32] and that Ireland was completely covered in ice from circa 27–23 kya [29, 31]. Details of the Irish bear samples and ancient DNA sequencing are provided in Table S2.

Figure 4. Three Hypothetical Scenarios Describing the Divergence between Brown Bear and Polar Bear Matrilines

(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.