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.

Phylogenomic evidence for ancient hybridization in the genomes of living cats (Felidae)

“…Although phylogenetic discordance is often attributed to ILS, the low effective population size of mitochondrial and Y Chromosome DNA, and that of felid species in general, coupled with the influence of male-mediated dispersal and Haldane's Rule on introgression, suggests that the conflicting phylogenetic signals between genomic partitions are best explained by hybridization (Currat et al 2008;Petit and Excoffier 2009;Cahill et al 2013). Our observations of historical admixture between many pairs of cat species are consistent with evidence for contemporary inter-specific hybridization in nature and captivity spanning large phylogenetic distances.…”

“…There is an emerging consensus that gene flow frequently occurs following speciation despite the establishment of reproductive barriers that otherwise maintain species-level distinctiveness (Roca et al 2005;Good et al 2008;Ellegren et al 2012;Garrigan et al 2012;Toews and Brelsford 2012;Cahill et al 2013Cahill et al , 2014Cui et al 2013;Martin et al 2013;Kutschera et al 2014;Sullivan et al 2014). However, incomplete lineage sorting (ILS) is assumed by default to underpin most cases of phylogenetic discordance.…”

“…However, incomplete lineage sorting (ILS) is assumed by default to underpin most cases of phylogenetic discordance. Few studies in the literature account for hybridization by analyzing all inheritance patterns (uniparental, sex-biased, biparental) with high-resolution data, or instead have focused on only a few species (Roca et al 2005;Cahill et al 2013Cahill et al , 2014Trigo et al 2013;Khan et al 2014). The cat family Felidae contains 38 recognized species within eight lineages (designated henceforth by a capitalized name, e.g., Puma lineage) that vary in the breadth of their geographic occurrence (Buckley-Beason et al 2006;Johnson et al 2006).…”

“…ABBA/BABA tests performed on the SNP data set included heterozygous sites by generating pseudohaploid sequences, following Green et al (2010) and Cahill et al (2013Cahill et al ( , 2014. Statistical significance of the Z-score was assessed for each replicate by converting the Z-score into a two-tailed P-value (Eaton and Ree 2013).…”

“…One thousand bootstrap iterations were used to measure the standard deviation of the D-statistic derived from the SNP-array data, because the ABBA/BABA SNP sites are largely unlinked (∼1 SNP per 4 Mb) (Eaton andRee 2013, Streicher et al 2014). We defined significant D-statistics as those having Z-scores ≥ 3 (following Green et al 2010;Cahill et al 2013). …”