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-κB 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.

Metabolic response of dolphins to short-term fasting reveals physiological changes that differ from the traditional fasting model

“…This is consistent with the emergence from differential expression of pathways in the present study [e.g. significant reduction in nervonate, which has been associated with insulin resistance ( Yamazaki et al, 2014 )], previous experimental work ( Venn-Watson et al, 2011 ) and comparative genomic studies ( Derous et al, 2021 ) that suggest fasting bottlenose dolphins protect circulating glucose from oxidative pathways. IL-10 signalling was also well represented in the DNM and may be an early signaller to the JAK/STAT pathway.…”

“…Yamazaki et al, 2014), previous experimental work(Venn-Watson et al, 2011) and comparative genomic studies(Derous et al, 2019) that suggest fasting bottlenose dolphins protect circulating glucose from oxidative pathways. IL-10 signalling was also well-represented in the DNM and may be an early signaller to the JAK/STAT pathway.…”

Toward New Ecologically Relevant Markers of Health for Cetaceans

“…Positive gene selection in energy metabolism-related biological pathways suggests these genes may have been positively selected to adapt to a glucosepoor diet and it is unlikely that fat depots signaling function in the same manner as in terrestrial mammals. Specifically adiposity is not likely to have the deleterious health consequences known in terrestrial mammals (Derous et al, 2019). For example, while low blubber thickness negatively impacted pregnancy rate in North Atlantic fin whales, larger than normal blubber thickness was still associated with the same rate of pregnancy as that of typical healthy animals (Williams et al, 2013).…”

“…In a land mammal, large volume of adipose tissue triggers inflammatory responses and can lead to metabolic dysfunctions at a physiological level (Mantovani et al, 2002). In cetaceans, key genes related to inflammation are positively selected in such a way that fat deposits signaling may not be as limited by inflammation, metabolic dysfunctions and reproduction (Derous et al, 2019). These phylogenomic studies indicate that due to evolutionary constraints associated with secondary adaptations to life in water, we cannot expect adipose signaling to interact with energy metabolism in cetaceans like it does in the classical mammalian model.…”

“…Fat stores not only play a role in maintaining energy balance, but also play a crucial signaling role to other organs to regulate energy metabolism (Trayhurn and Beattie, 2007;Ye, 2011). There are indications that some of these signaling functions have changed during the evolutionary trajectory of these species (Ball et al, 2017;Derous et al, 2019). Crucially, these adaptations impact the ways in which individuals decide to invest in reproduction and define their abilities to survive under varied environmental pressures.…”