Physiology and Behavior Influence Lactation Efficiency in Northern Elephant Seals ( Mirounga angustirostris )

SUMMARYThe northern elephant seal pup (Mirounga angustirostris) undergoes a 2-3month post-weaning fast, during which it depends primarily on the oxidation of fatty acids to meet its energetic demands. The concentration of non-esterified fatty acids (NEFAs) increases and is associated with the development of insulin resistance in late-fasted pups. Furthermore, plasma NEFA concentrations respond differentially to an intravenous glucose tolerance test (ivGTT) depending on fasting duration, suggesting that the effects of glucose on lipid metabolism are altered. However, elucidation of the lipolytic mechanisms including lipase activity during prolonged fasting in mammals is scarce. To assess the impact of fasting and glucose on the regulation of lipid metabolism, adipose tissue and plasma samples were collected before and after ivGTTs performed on early (2weeks, N5) and late (6-8weeks; N8) fasted pups. Glucose administration increased plasma triglycerides and NEFA concentrations in late-fasted seals, but not plasma glycerol. Fasting decreased basal adipose lipase activity by 50%. Fasting also increased plasma lipase activity twofold and decreased the expressions of CD36, FAS, FATP1 and PEPCK-C by 22-43% in adipose tissue. Plasma acylcarnitine profiling indicated that late-fasted seals display higher incomplete LCFA -oxidation. Results suggest that long-term fasting induces shifts in the regulation of lipolysis and lipid metabolism associated with the onset of insulin resistance in northern elephant seal pups. Delineation of the mechanisms responsible for this shift in regulation during fasting can contribute to a more thorough understanding of the changes in lipid metabolism associated with dyslipidemia and insulin resistance in mammals.

Section: Discussionmentioning

confidence: 99%

Decreased expression of adipose CD36 and FATP1 are associated with increased plasma non-esterified fatty acids during prolonged fasting in northern elephant seal pups (Mirounga angustirostris)

Viscarra

Vázquez‐Medina

Rodríguez

et al. 2012

“…Although shortterm elevations of NEFA are known to stimulate insulin secretion (Bollheimer et al, 1998), a considerable amount of research has shown that chronically elevated NEFA are the initiating cause of an impairment in insulin signal transduction (Boden and Laakso, 2004;Yu et al, 2002). Previous research has shown that fasting elephant seals have elevated NEFA (1.0-3.2 mmol l -1 ) (Castellini et al, 1987;Houser et al, 2007;McDonald and Crocker, 2006) in comparison to other non-fasting adapted species (e.g. 0.14 mmol l -1 in humans) (Fery et al, 1990).…”

Section: Mechanisms For Altering Insulin Secretion and Sensitivitymentioning

confidence: 99%

Hormonal regulation of glucose clearance in lactating northern elephant seals (Mirounga angustirostris)

Fowler

Champagne

Houser

et al. 2008

SUMMARYNorthern elephant seals exhibit the rare strategy of fasting and lactating concomitantly. We investigated hormonal regulation of glucose clearance in northern elephant seals using glucose tolerance tests (GTT) performed early in lactation and again just prior to weaning. For comparison, identical measurements were made on separate females late in the molt fast. Serial blood samples were used to assess glucose clearance and hormone responses for 3 h post glucose injection. Plasma glucose remained elevated at the end of the sampling period in all groups. Glucose clearance rates were not significantly different among test groups. A significant insulin response was observed in early lactation, no significant response was observed late in lactation and an intermediate response was observed late in the molt fast. The insulin response to a glucose load decreased with adipose tissue proportions. Plasma glucagon decreased significantly following GTT in early and late lactation, although the magnitude of the depression was small in comparison to other species. Hypoinsulemia may be critical to facilitate net lipolysis late in lactation. Consistently low glucose clearance among test groups suggests insulin insensitivity within peripheral tissues. Glucagon suppression independent of insulin release suggests modification of the typical insulin-glucagon counter-regulation. These findings suggest that metabolic features of diabetic-like conditions may be adaptive in the context of long-term fasting.

“…During the breeding season, female NES give birth to a single pup and nurse the pup for ∼26 days while abstaining completely from nutrient intake. This intense, short investment period is characterized by rapid nutrient transfer from mother to pup in the form of milk that is ∼25% lipid in early lactation, increasing to >55% lipid shortly before weaning (McDonald and Crocker, 2006;Fowler et al, 2016;Crocker et al, 2001) (Table 1, Fig. 1).…”

mentioning

confidence: 99%

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

Fowler

Champagne

Crocker

2018

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.