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. 2017 Jan;187(1):235-252.
doi: 10.1007/s00360-016-1029-6. Epub 2016 Aug 29.

Beyond Thermoregulation: Metabolic Function of Cetacean Blubber in Migrating Bowhead and Beluga Whales

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Free PMC article

Beyond Thermoregulation: Metabolic Function of Cetacean Blubber in Migrating Bowhead and Beluga Whales

H C Ball et al. J Comp Physiol B. .
Free PMC article

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 the 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.

Keywords: Blubber; Bowhead whale; Development; Leptin; Metabolic activity.

Conflict of interest statement

Competing Interests

Conflict of Interest: The authors declare that they have no conflict of interest.

Figures

Fig 1
Fig 1. Bowhead and belugas share bi-annual migratory routes but bowheads likely experience more dramatic seasonal shifts in feeding patterns
Migration in both species occurs as a result of increasing sea ice cover and decreasing daylight in the Autumn. While beluga whales are pelagic and benthic feeders with probably more frequent feeding bouts, bowheads experience caloric restriction and dramatic, seasonal shifts in feeding due to differences in Arctic productivity (Quakenbush et al. 2010 and Citta et al. 2012)
Fig 2
Fig 2. Seasonal and Ontogenetic Differences in transcripts of Lep and LEPR-b, but not conserved LEPR, in bowhead and beluga whales
Leptin, conserved LEPR and LEPR-b transcript levels differ significantly with age in bowhead (A–C) and beluga (D–F) whales and also with season in bowheads. Transcripts levels were measured per equivalent amounts of starting RNA sampled from subcutaneous adipose. Error bars depict 95% confidence intervals
Fig 3
Fig 3. Seasonal and Ontogenetic Differences in Lipolytic Activity of bowhead and beluga whales
Analyses detected significant differences in PNPLA2 and LIPE transcript levels with season and age in bowhead, but not beluga, whales. Transcripts levels were measured per equivalent amounts of starting RNA sampled from subcutaneous adipose. Error bars depict 95% confidence intervals.
Fig 4
Fig 4. Measurements of Leptin titer (pg/µl) from bowhead sera correlated with seasonal and ontogenetic changes in mRNA expression of bowhead whales
Seasonal and ontogenetic variations in Leptin titer were measured from sera of mature and sub-adult Fall bowheads and three Spring sub-adults. Assays were conducted using a heterologous assay. Error bars depict 95% confidence intervals
Fig 5
Fig 5. Dynamic model simulation comparisons of human, beluga and bowhead Leptins
(A) Homology models for human (gray), beluga whale (cyan), and bowhead whale (magenta) aligned to the solved NMR structure of human Leptin (pdb file 1ax8). (B) Molecular dynamic simulations of each model and also that of the closely related cow Leptin. (C) Variants (blue) between beluga and bowhead Leptin proteins (gray) shown relative to the binding pocket with LEPR-b (cyan). (D) Amino acids differences between human and the whale Leptin proteins shown for the interface between Leptin (gray) and LEPR-b (cyan) interactions
Fig 6
Fig 6. Bowheads demonstrate extreme Lep transcript variation with age and season
This multispecies comparison illustrates beluga whales, demonstrate slight variation in Lep transcripts with age and physiology. Bowheads are unique among mammals: adults in the Fall display a greater than two-fold higher expression than same season youths and Spring mature and sub-adults. This is unique because all cetaceans possess large adipose reserves regardless of age or season. Measurements of Lep transcripts number were from equivalent amounts of starting total RNA and error bars depict 95% confidence intervals

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