Chromosome-scale genomes show rapid diversification and ancient gene flow among bear species

Abstract

Reconstructions of evolutionary history can be restricted by a lack of high quality reference genomes. To-date, only four of the eight species of bears (family Ursidae) have chromosome-level genome assemblies. Here, we present assemblies for three additional species - the sun, sloth, and spectacled bears - and use a whole-genome alignment of all bear species and other carnivores to reconstruct the evolution of Ursidae. Divergence dating based on patterns of coalescence indicates a more rapid diversification than previously reported, with a ∼19 Ma origin for all bears but a ∼3.3 Ma origin for the six species of the subfamily Ursinae. Surprisingly, we observe that nearly 50% of gene tree topologies conflict with our highly supported species tree, a pattern driven by a significant early hybridization event within Ursinae. We also find that the ancestral karyotype of Ursinae has remained largely conserved with the ancestral karyotype of all bears over roughly fifteen million years. In contrast to this stability, dozens of chromosomal fissions and fusions associated with LINE/L1 retrotransposons dramatically restructured the genomes of the giant panda and spectacled bear. Finally, we leverage these genomes to identify species-specific evidence for positive selection on genes associated with color, diet, and metabolism. One of these genes, TCPN2, has a role in pigmentation and shows a series of amino acid mutations in the polar bear over the last 0.5 Ma. Collectively, these new genomic resources enable improved reconstruction of the complex evolutionary history of bears and clarify how this enigmatic group diversified.

Keywords: Bears; chromosome evolution; gene flow; phylogenomics; positive selection.