Polar bears exhibit genome-wide signatures of bioenergetic adaptation to life in the arctic environment

Abstract

Polar bears (Ursus maritimus) face extremely cold temperatures and periods of fasting, which might result in more severe energetic challenges than those experienced by their sister species, the brown bear (U. arctos). We have examined the mitochondrial and nuclear genomes of polar and brown bears to investigate whether polar bears demonstrate lineage-specific signals of molecular adaptation in genes associated with cellular respiration/energy production. We observed increased evolutionary rates in the mitochondrial cytochrome c oxidase I gene in polar but not brown bears. An amino acid substitution occurred near the interaction site with a nuclear-encoded subunit of the cytochrome c oxidase complex and was predicted to lead to a functional change, although the significance of this remains unclear. The nuclear genomes of brown and polar bears demonstrate different adaptations related to cellular respiration. Analyses of the genomes of brown bears exhibited substitutions that may alter the function of proteins that regulate glucose uptake, which could be beneficial when feeding on carbohydrate-dominated diets during hyperphagia, followed by fasting during hibernation. In polar bears, genes demonstrating signatures of functional divergence and those potentially under positive selection were enriched in functions related to production of nitric oxide (NO), which can regulate energy production in several different ways. This suggests that polar bears may be able to fine-tune intracellular levels of NO as an adaptive response to control trade-offs between energy production in the form of adenosine triphosphate versus generation of heat (thermogenesis).

Keywords: cellular respiration; mitochondrial genome; nitric oxide; nuclear genome; oxidative phosphorylation.

Fig. 1.—

Discordance among mitochondrial and nuclear phylogenies for brown and polar bears. The dashed line is a diagrammatic representation of the mitochondrial gene tree, in which brown bears are paraphyletic. Thick black lines represent the nuclear gene tree, in which brown and polar bears form reciprocally monophyletic groups.

Fig. 2.—

Overview of methods used to investigate the nuclear genomes of brown and polar bears for adaptations related to cellular respiration. The allele present in two of the three bear species was assumed to be ancestral. For example, a derived allele in polar bear would differ from the alleles found in brown and black bears. Dark gray indicates analysis of function, and light gray indicates analysis for positive selection. Bb is brown bear and Pb is polar bear.

Fig. 3.—

Structure of the bovine cytochrome c oxidase complex. (A) Amino acid position 57 of COXI is highlighted in orange. This position occurs near predicted heme-binding sites at positions 54, 58, and 61–62. (B) Amino acid position 512 of COXI protein is highlighted in green and surrounded by beta-pleated sheets of the nuclear-encoded subunit Vb protein.