Polar bear evolution is marked by rapid changes in gene copy number in response to dietary shift

Abstract

Polar bear (Ursus maritimus) and brown bear (Ursus arctos) are recently diverged species that inhabit vastly differing habitats. Thus, analysis of the polar bear and brown bear genomes represents a unique opportunity to investigate the evolutionary mechanisms and genetic underpinnings of rapid ecological adaptation in mammals. Copy number (CN) differences in genomic regions between closely related species can underlie adaptive phenotypes and this form of genetic variation has not been explored in the context of polar bear evolution. Here, we analyzed the CN profiles of 17 polar bears, 9 brown bears, and 2 black bears (Ursus americanus). We identified an average of 318 genes per individual that showed evidence of CN variation (CNV). Nearly 200 genes displayed species-specific CN differences between polar bear and brown bear species. Principal component analysis of gene CN provides strong evidence that CNV evolved rapidly in the polar bear lineage and mainly resulted in CN loss. Olfactory receptors composed 47% of CN differentiated genes, with the majority of these genes being at lower CN in the polar bear. Additionally, we found significantly fewer copies of several genes involved in fatty acid metabolism as well as AMY1B, the salivary amylase-encoding gene in the polar bear. These results suggest that natural selection shaped patterns of CNV in response to the transition from an omnivorous to primarily carnivorous diet during polar bear evolution. Our analyses of CNV shed light on the genomic underpinnings of ecological adaptation during polar bear evolution.

Keywords: adaptive evolution; copy number variation; population genomics.

Fig. 1.

Genes with differentiated CN profiles between polar bear and brown bear. (Lower) A Manhattan plot of V_ST values (y axis) for each gene (n = 21,142) (x axis) in the reference polar bear genome. Genes are depicted by their V_ST value patterns across the Control-FREEC and BDN CN estimations: red = V_ST > 0.35 in both CN estimation methods, purple = V_ST > 0.22 and V_ST ≤ 0.35 in both CN estimation methods, blue = V_ST > 0.22 in one CN estimation method and V_ST > 0.35 in the other CN estimation, and gray = V_ST ≤ 0.22 in at one or both CN estimation methods. Genes of interest are labeled according to their respective human annotations, and are highlighted with gray boxes. (Upper) A heat map of diploid gene CN (columns) for each of the 197 differentiated genes in the 17 polar bear individuals, 9 brown bear individuals, and 2 black bear individual (rows). Genes with black circle notations represent high-CN genes and have different scales (see key). Black and yellow represent a CN of zero, and a high CN (8 or 50 depending on scale), respectively. Polar bear gene identifiers, along with either human or dog annotations when available, are noted for each gene. CNs are from Control-FREEC estimates. Individual samples identifiers and gene identifiers are provided in Dataset S1.

Fig. 2.

Polar bear possess fewer copies of AMY1B compared with brown bear. Box and whisker plot of gene CN for the salivary amylase-encoding gene, AMY1B (A). CNs are from Control-FREEC estimates. Each dot represents the diploid CN (y axis) for a given bear individual (x axis). The box plot displays the median value, first quartile, and third quartile. Whiskers are drawn to the furthest point with 1.5× the interquartile range (third quartile minus the first quartile) from the box. The black bear does not include a box and whisker plot because the analysis included only two individuals. (B) A heat map depicting the BDN CN estimates for nonoverlapping 100-bp windows in the AMY2B and AMY1B locus on scaffold70 (positions 1,331,300 to 1,380,700) of the reference polar bear genome.

Fig. 3.

Polar bear exhibits divergent CN profiles compared with brown bear and black bear. PCA of gene CN across all bear individuals for genes showing agreement between the two CN estimation methods. (A) All CN-variable genes (V_ST > 0; 4,698 genes), (B) differentiated genes (V_ST > 0.22; 197 genes), and (C) highly differentiated genes (V_ST > 0.35; 134 genes). The percentage of variance explained by PC1, PC2, and PC3 are provided below each plot.