Adiposity and fat metabolism during combined fasting and lactation in elephant seals

Abstract

Animals that fast depend on mobilizing lipid stores to power metabolism. Northern elephant seals (Mirounga angustirostris) incorporate extended fasting into several life-history stages: development, molting, breeding and lactation. The physiological processes enabling fasting and lactation are important in the context of the ecology and life history of elephant seals. The rare combination of fasting and lactation depends on the efficient mobilization of lipid from adipose stores and its direction into milk production. The mother elephant seal must ration her finite body stores to power maintenance metabolism, as well as to produce large quantities of lipid and proteinrich milk. Lipid from body stores must first be mobilized; the action of lipolytic enzymes and hormones stimulate the release of fatty acids into the bloodstream. Biochemical processes affect the release of specific fatty acids in a predictable manner, and the pattern of release from lipid stores is closely reflected in the fatty acid content of the milk lipid. The content of the milk may have substantial developmental, thermoregulatory and metabolic consequences for the pup. The lactation and developmental patterns found in elephant seals are similar in some respects to those of other mammals; however, even within the limited number of mammals that simultaneously fast and lactate, there are important differences in the mechanisms that regulate lipid mobilization and milk lipid content. Although ungulates and humans do not fast during lactation, there are interesting comparisons to these groups regarding lipid mobilization and milk lipid content patterns.

Expression of obesity-related adipokine genes during fasting in a naturally obese marine mammal

“…Weight loss and corticosteroid hormones. Females sampled late in lactation and molting had lower mass and adiposity and elevated circulating corticosteroid levels relative to early fasting groups, consistent with other studies in this species and the known lipolytic and gluconeogenic functions of cortisol that are required to support fasting metabolism (4,7,16). The highest corticosteroid concentrations were measured in late lactation, when milk lipid concentration is highest (16), while the lowest were measured during early molt, when females return from their postbreeding foraging trip.…”

“…Females sampled late in lactation and molting had lower mass and adiposity and elevated circulating corticosteroid levels relative to early fasting groups, consistent with other studies in this species and the known lipolytic and gluconeogenic functions of cortisol that are required to support fasting metabolism (4,7,16). The highest corticosteroid concentrations were measured in late lactation, when milk lipid concentration is highest (16), while the lowest were measured during early molt, when females return from their postbreeding foraging trip. Gains in mass and adiposity were higher during the postmolting foraging trip, which is associated with gestation, than during the postbreeding foraging trip, when females mainly replenish protein stores impacted by lactation (1,9,37).…”

“…However, adipokine responses to fasting vary by species, life history stage, sex, and tissue type, and much remains unknown. For example, adipokines have never been measured in adult female elephant seals during their lactation fast, when they produce one of the most energy-dense milks in nature (up to 55% fat) using solely their lipid stores in blubber (16,35). This energy-demanding fasting period has also been associated with innate and adaptive immune responses to breeding in a dense colonial environment (33).…”

A blubber gene expression index for evaluating stress in marine mammals

“…Body CI was negatively associated with cortisol and rT3, which is consistent with a previous study of juvenile elephant seals that found that T4 levels significantly decreased over a fasting period during which animals lost 17% of their body fat ( Kelso et al , 2012 ). Cortisol was also negatively associated with adiposity in lactating adult female elephant seals ( Fowler et al , 2018 ), but not in juveniles ( Kelso et al , 2012 ), highlighting the importance of evaluating stress state in the context of life history stage, especially in fasting-adapted marine mammals. Body condition was also negatively associated with DKK1 , but not with any of the other gene markers, suggesting that this gene may be a novel molecular marker of adiposity in marine mammals.…”

Changes in Northern Elephant Seal Skeletal Muscle Following Thirty Days of Fasting and Reduced Activity

“…Northern elephant seals (NES) have an annual cycle that includes months at sea foraging and acquiring body fat, punctuated by extended fasting periods while hauled out on land for molting or pupping/breeding ( Fowler et al, 2018 ). When molting, these seals typically spend ∼40 days on land with the combined catabolic stimuli to skeletal muscle of reduced activity and fasting.…”