Genomic evidence for island population conversion resolves conflicting theories of polar bear evolution

Abstract

Despite extensive genetic analysis, the evolutionary relationship between polar bears (Ursus maritimus) and brown bears (U. arctos) remains unclear. The two most recent comprehensive reports indicate a recent divergence with little subsequent admixture or a much more ancient divergence followed by extensive admixture. At the center of this controversy are the Alaskan ABC Islands brown bears that show evidence of shared ancestry with polar bears. We present an analysis of genome-wide sequence data for seven polar bears, one ABC Islands brown bear, one mainland Alaskan brown bear, and a black bear (U. americanus), plus recently published datasets from other bears. Surprisingly, we find clear evidence for gene flow from polar bears into ABC Islands brown bears but no evidence of gene flow from brown bears into polar bears. Importantly, while polar bears contributed <1% of the autosomal genome of the ABC Islands brown bear, they contributed 6.5% of the X chromosome. The magnitude of sex-biased polar bear ancestry and the clear direction of gene flow suggest a model wherein the enigmatic ABC Island brown bears are the descendants of a polar bear population that was gradually converted into brown bears via male-dominated brown bear admixture. We present a model that reconciles heretofore conflicting genetic observations. We posit that the enigmatic ABC Islands brown bears derive from a population of polar bears likely stranded by the receding ice at the end of the last glacial period. Since then, male brown bear migration onto the island has gradually converted these bears into an admixed population whose phenotype and genotype are principally brown bear, except at mtDNA and X-linked loci. This process of genome erosion and conversion may be a common outcome when climate change or other forces cause a population to become isolated and then overrun by species with which it can hybridize.

Figure 1. Map showing the approximate current geographic ranges of brown bears (brown) and polar bears (blue).

Numbers indicate the geographic location of origin of two brown bears and seven polar bears analyzed here. An American black bear from central Pennsylvania was also sequenced as part of this study. Shotgun data amounting to 4–6× coverage for polar bears and 11–12× coverage for brown and black bears (Table S2) was aligned to the current distribution of the polar bear genome .

Figure 2. Genetic diversity within and between bear species.

(A) Pairwise differences between individuals estimated as the average number of differences per 10 thousand bases (kb) in 42,000 non-overlapping 50 kb regions. After strict quality filtering, within-sample heterozygosity was resolved by selecting a single, high-quality base at random. The Lancaster Sound polar bear showed an excess of postmortem damage, as expected for historic specimens , and is shown in Figure S1. Polar bears are remarkably homogenous compared to brown bears, and both polar bears and brown bears are approximately equally diverged from the American black bear. Consistent with the results of the D-statistic test, pairwise distance between the ABC Islands brown bear and all polar bears (yellow lines) is less than that between the mainland brown bear and all polar bears (red lines). (B) Schematic diagram of a representative gene tree within brown bear, polar bear, and black bear populations, with the present day at the left of the diagram. For this locus, admixture occurring more recently than the population divergence of polar bears leads to the introgression of a polar bear haplotype into brown bears. Estimate of average genomic distance for brown, black, and polar bears and for population divergence between brown bears and polar bears given different calibration points are provided in Table 1.

Figure 3. Summary of D-statistic comparisons between polar bears and brown bears.

In each comparison, the black bear was used to define the ancestral allele. The Z-score of the D-statistic for each comparison is shown for autosomes (red) and X-chromosome (blue). Each dot represents the data from comparison of one pair of bears. In the top panel, all pairs of polar bears are compared for excess derived allele matching against the mainland brown bear. In the middle panel, all pairs of polar bears are compared against the ABC Island brown bear. The bottom panel shows the comparison of the two brown bears for excess allele matching to polar bears with each dot representing a different polar bear.

Figure 4. Simulated admixture reveals the direction of gene flow on the X chromosome.

(A) Pairwise distance as in Figure 2 but limited to the 12 scaffolds identified as X-chromosome. (B) 100 replicate simulations in which 6.5% of the female West Hudson Bay polar bear X-chromosome is replaced with that of the mainland Alaska brown bear in randomly inserted 20 kb fragments, simulating admixture from the brown bear genome into polar bear ∼50kya. Pairwise differences are calculated between the simulated genome (light brown lines; mean highlighted in dark brown) and the plot comparing the two female polar bears (blue line), to maximize the number of informative sites in the test. The addition of brown bear DNA to the polar bear genome markedly increases the number of high-diversity bins (>10 differences/10 kb), indicating that any introgression of brown bear DNA into polar bears should be easily detectable. (C). As in (B), but with 6.5% of the mainland Alaska brown bear X-chromosome is replaced with that of the female West Hudson Bay polar bear. In this instance, we find no difference between the simulated (blue lines) and real (brown line) data.