Research Article: Genomic Evidence for Island Population Conversion Resolves Conflicting Theories of Polar Bear Evolution

Date Published: March 14, 2013

Publisher: Public Library of Science

Author(s): James A. Cahill, Richard E. Green, Tara L. Fulton, Mathias Stiller, Flora Jay, Nikita Ovsyanikov, Rauf Salamzade, John St. John, Ian Stirling, Montgomery Slatkin, Beth Shapiro, Michael W. Nachman

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.

Partial Text: Despite polar bears’ clear morphological and behavioral adaptations to their arctic environment [1], [2], their genetic relationship to brown bears remains unclear [3], [4], [5], [6]. Analysis of maternally inherited mitochondrial DNA (mtDNA) shows that polar bears fall within the range of variation of brown bears. Extant brown bears from Alaska’s ABC (Admiralty, Baranof and Chichagof) Islands, some extinct brown bears from Ireland and mainland Alaska, and two ∼115,000-year-old polar bears share the mtDNA haplotype of all extant polar bears [3], [7], [8], [9], [10], [11]. The time to most recent common ancestor (TMRCA) of this mtDNA haplotype has been estimated at ∼160 thousand years ago (kya) (Figure S7) [3], [6], [9], [10]. Recent analysis of data from a panel of brown and polar bears at 14 nuclear loci showed that polar bears are generally distinct from brown bears, with genomic TMRCA averaging ∼600 kya [4]. Under a simple population split model without subsequent admixture, the population divergence should be more recent than average genomic divergence and thus polar bears became a distinct species more recently than 600 kya. A separate recent genome sequencing survey concluded that brown bear and polar bear lineages are much older. Miller and colleagues concluded that the lineage that would become polar bears diverged from that which would become brown bears more than 4 million years ago, followed by admixture that continues to the present [6]. Consistent with this, the past and present geographic ranges of both species overlap at their margins (Figure 1), and fertile hybrids are known in both captive and wild populations [2], [12].

To more fully delineate the genetic relationship between polar bears and brown bears, we sequenced random genomic shotgun libraries from seven polar bears, two brown bears and one black bear to learn the ancestral state for alleles (Figure 1, Text S1). We mapped these reads to the assembled genome scaffolds of polar bear (Text S1) [13]. Because the sequence coverage of each bear was uneven and too low to reliably call heterozygous sites, we down-sampled the sequence data from each bear to 1×. That is, we randomly picked a high-quality base from amongst all reads that mapped reliably at each position in the bear genome. In this way, we generated a composite haplotype for each bear and used these data for further analysis.

The genome-wide analysis presented here indicates that (1) polar bears are a remarkably homogeneous species and show no evidence of brown bear ancestry, (2) the ABC Islands brown bears show clear evidence of polar bear ancestry, and (3) this polar bear ancestry of ABC Islands brown bears is conspicuously enriched in the X-chromosome. ABC Islands brown bears show a simple positive correlation between how maternally biased a genetic locus is (mtDNA>X chromosome>autosomes) and how much polar bear ancestry is present (100%, 6.5%, 1%). Given this observation, and our knowledge about the natural history of these islands through the Pleistocene and Holocene, we present the following model.

We extracted DNA from nine of the ten bears in a modern DNA laboratory using the DNeasy Blood & Tissue Kit (Qiagen) according to the manufacturer’s specifications. The historic Lancaster Sound polar bear (Smithsonian Natural History Museum ID 512133; Table S1) was extracted in a dedicated ancient DNA laboratory at Penn State University that is geographically isolated from modern molecular biology research, using a column-based extraction protocol for ancient DNA [25].