Adaptations of energy metabolism in cetaceans have consequences for their response to foraging disruption

Abstract

Cetaceans have varied their anatomical structure, physiology and metabolism to adapt to the challenges of aquatic life. Key to this change is the deposition of blubber. This adipose tissue plays a significant regulatory and signaling role in mammalian metabolism. As foraging disruption by human activities is emerging as a key conservation threat for cetaceans, we need to understand how selection for aquatic life might have altered key nutrient sensing pathways associated with adipose signaling. We compared selection pressure on those energy metabolism biological pathways by contrasting the rate of substitution observed in genes associated with them in cetacean and artiodactyl genomes. We then estimated the likely consequence of these selection pressures for pathway functions. Here we show that genes involved in the insulin, mTOR, SIRT and NF-{kappa}B pathways were under significant positive selection in cetaceans compared to their terrestrial sister taxon. Our results suggest these genes may have been positively selected to adapt to a glucose-poor diet and it is unlikely that fat depots signaling function in the same manner as in terrestrial mammals. Secondary adaptation to life in water significantly affected functions in nutrient sensing pathways in cetaceans. Insulin is not likely to play the same role in energy balance as it does in terrestrial mammals and adiposity is not likely to have the deleterious health consequences it has in terrestrial mammals. The physiological ecology of cetacean fat deposition, and therefore its value as a condition index, needs to be interpreted in this evolutionary context.