Beyond thermoregulation: metabolic function of cetacean blubber in migrating bowhead and beluga whales

Abstract

The processes of lipid deposition and utilization, via the gene leptin (Lep), are poorly understood in taxa with varying degrees of adipose storage. This study examines how these systems may have adapted in marine aquatic environments inhabited by cetaceans. Bowhead (Balaena mysticetus) and beluga whales (Delphinapterus leucas) are ideal study animals- they possess large subcutaneous adipose stores (blubber) and undergo bi-annual migrations concurrent with variations in food availability. To answer long-standing questions regarding how (or if) energy and lipid utilization adapted to aquatic stressors, we quantified variations in gene transcripts critical to lipid metabolism related to season, age and blubber depth. We predicted Leptin tertiary structure conservation and assessed inter-specific variations in Lep transcript numbers between bowheads and other mammals. Our study is the first to identify seasonal and age-related variations in Lep and lipolysis in these cetaceans. While Lep transcripts and protein oscillate with season in adult bowheads reminiscent of hibernating mammals, transcript levels reach up to 10-times higher in bowheads than any other mammal. Data from immature bowheads are consistent with the hypothesis that short baleen inhibits efficient feeding. Lipolysis transcripts also indicate young Fall bowheads and those sampled during Spring months limit energy utilization. These novel data from rarely examined species expand existing knowledge and offer unique insight into how the regulation of Lep and lipolysis has adapted to permit seasonal deposition and maintain vital blubber stores.

On the Molecular Evolution of Leptin, Leptin Receptor, and Endospanin

“…Although leptin is thought to drive the prehibernation anorexia of some, but not all hibernating mammals [reviewed in Ref. (117)], organisms with life histories that are distinctly seasonal (but not necessarily hibernating) may change their set point for leptin sensitivity to accommodate different levels of activity and food availability between seasons (97, 112, 118, 119); thus, an adipostat as described for rodents may not be adaptive for fishes.…”

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

“…The processes of lipid deposition and utilization is regulated by the gene leptin (LEP) (Duncan et al, 2007). Recent work shows that in bowhead whales ( Balaena mysticetus ) and belugas ( Delphinapterus leucas ), the regulation of LEP and lipolysis is adapted to seasonal cycles of blubber deposition and utilization (Ball et al, 2017). Although adipose tissue biology of terrestrial mammals show a similarity to the functioning of cetacean blubber, some differences in key genes have been identified (Ball et al, 2017).…”

“…Recent work shows that in bowhead whales ( Balaena mysticetus ) and belugas ( Delphinapterus leucas ), the regulation of LEP and lipolysis is adapted to seasonal cycles of blubber deposition and utilization (Ball et al, 2017). Although adipose tissue biology of terrestrial mammals show a similarity to the functioning of cetacean blubber, some differences in key genes have been identified (Ball et al, 2017). These changes have therefore the scope to alter the way individual take biological decisions about demographic contributions, particularly reproduction, given their energetic metabolic state.…”

Review and experimental evaluation of the embryonic development and evolutionary history of flipper development and hyperphalangy in dolphins (Cetacea: Mammalia)

“…Because of the lack of fresh and sustainable sources of tissues of cetaceans that display the extreme phenotype of hyperphalangy, it may only be feasible for future exploration to identify the mechanism driving this minor form of hyperphalangy. Ongoing work could utilize tissues of Delphinapterus and Balaena as they display this minor form of hyperphalangy and are currently used to study molecular and anatomical adaptations associated with bone development (Thewissen et al, ), sensory biology (Drake, Crish, George, Stimmelmayr, & Thewissen, ; Sensor et al, ), and physiology (Ball et al, ; George et al, ). Furthermore, augmentation of these developmental data with direct evidence of their biomechanical consequences would link gene function to phenotype and add insight into how a given morphological trait can influence performance within a complex, three‐dimensional environment.…”