Terrestrial Birth and Body Size Tune UCP1 Functionality in Seals.

The molecular evolution of the mammalian heater protein UCP1 is a powerful biomarker to understand thermoregulatory strategies during species radiation into extreme climates, such as aquatic life with high thermal conductivity. While fully aquatic mammals lost UCP1, most semiaquatic seals display intact UCP1 genes, apart from large elephant seals. Here, we show that UCP1 thermogenic activity of the small-bodied harbor seal is equally potent compared to terrestrial orthologs, emphasizing its importance for neonatal survival on land. In contrast, elephant seal UCP1 does not display thermogenic activity, not even when translating a repaired or a recently highlighted truncated version. Thus, the thermogenic benefits for neonatal survival during terrestrial birth in semiaquatic pinnipeds maintained evolutionary selection pressure on UCP1 function and were only outweighed by extreme body sizes among elephant seals, fully eliminating UCP1-dependent thermogenesis.

Effects of cortisol, epinephrine, and bisphenol contaminants on the transcriptional landscape of marine mammal blubber.

Top ocean predators such as marine mammals are threatened by intensifying anthropogenic activity, and understanding the combined effects of multiple stressors on their physiology is critical for conservation efforts. We investigated potential interactions between stress hormones and bisphenol contaminants in a model marine mammal, the northern elephant seal (NES). We exposed precision-cut adipose tissue slices (PCATS) from blubber of weaned NES pups to cortisol (CORT), epinephrine (EPI), bisphenol A (BPA), bisphenol S (BPS), or their combinations (CORT-EPI, BPA-EPI, and BPS-EPI) ex vivo and identified hundreds of genes that were differentially regulated in response to these treatments. CORT altered expression of genes associated with lipolysis and adipogenesis, whereas EPI and CORT-EPI-regulated genes were associated with responses to hormones, lipid and protein turnover, immune function, and transcriptional and epigenetic regulation of gene expression, suggesting that EPI has wide-ranging and prolonged impacts on the transcriptional landscape and function of blubber. Bisphenol treatments alone had a weak impact on gene expression compared with stress hormones. However, the combination of EPI with bisphenols altered expression of genes associated with inflammation, cell stress, DNA damage, regulation of nuclear hormone receptor activity, cell cycle, mitochondrial function, primary ciliogenesis, and lipid metabolism in blubber. Our results suggest that CORT, EPI, bisphenols, and their combinations impact cellular, immune, and metabolic homeostasis in marine mammal blubber, which may affect the ability of marine mammals to sustain prolonged fasting during reproduction and migration, renew tissues, and mount appropriate responses to immune challenges and additional stressors.

In vitro Lipolysis and Leptin Production of Elephant Seal Blubber Using Precision-Cut Adipose Tissue Slices.

Adipose tissue plays key roles in energy homeostasis. Understanding its metabolism and regulation is essential to predict the impact of environmental changes on wildlife health, especially in fasting-adapted species. However, in vivo experimental work in wild vertebrates can be challenging. We have developed a novel in vitro approach of precision-cut adipose tissue slices from northern elephant seal (Mirounga angustirostris) as a complementary approach to whole animal models. Blubber biopsies were collected from 14 pups during early and late post-weaning fast (Año Nuevo, CA, United States), precision-cut into 1 mm thick slices and maintained in culture at 37°C for at least 63 h. The slices exhibited an efficient response to ß-adrenergic stimulation, even after 2 days of culture, revealing good in vitro tissue function. The response to lipolytic stimulus did not vary between regions of outer and inner blubber, but was higher at early than at late fast for inner blubber slices. At early fast, lipolysis significantly reduced leptin production. At this stage, inner blubber slices were also more efficient at producing leptin than outer blubber slices, especially in the non-lipolytic condition. This model will aid the study of adipose tissue metabolism and its response to environmental stressors in marine mammals.