Stockpiling by pups and self-sacrifice by their fasting mothers observed in birth to weaning serum metabolomes of Atlantic grey seals

Abstract

During the uniquely short lactations of true seals, pups acquire a greater proportion of maternal body resources, at a greater rate, than in any other group of mammals. Mothers in many species enter a period of anorexia but must preserve sufficient reserves to fuel hunting and thermoregulation for return to cold seas. Moreover, pups may undergo a period of development after weaning during which they have no maternal care or nutrition. This nutritionally closed system presents a potentially extreme case of conflict between maternal survival and adequate provisioning of offspring, likely presenting strains on their metabolisms. We examined the serum metabolomes of five mother and pup pairs of Atlantic grey seals, Halichoerus grypus, from birth to weaning. Changes with time were particularly evident in pups, with indications of strain in the fat and energy metabolisms of both. Crucially, pups accumulate certain compounds to levels that are dramatically greater than in mothers. These include compounds that pups cannot synthesise themselves, such as pyridoxine/vitamin B6, taurine, some essential amino acids, and a conditionally essential amino acid and its precursor. Fasting mothers therefore appear to mediate stockpiling of critical metabolites in their pups, potentially depleting their own reserves and prompting cessation of lactation.

Atlantic Grey Seal Milk Shows Continuous Changes in Key Metabolites and Indicators of Metabolic Transition in Pups From Birth to Weaning

“…There is therefore, no period that may be described as a stable, mature phase of lactation. Some of these changes may indicate an early switch from carbohydrate to fat metabolism in pups, and provisioning of pups beyond their immediate needs ("stockpiling") for their post-weaning fast (Watson et al, 2020). These new findings emphasize the dramatic adaptations, strains, and refinements in the evolution of lactation by Atlantic grey and other true seals as capital breeding, hypercarnivorous mammals that have moved from land to cold and frozen aquatic environments.…”

“…The darted animals were kept under observation from a distance for any difficulties for 10 min before approach (Langton et al, 2011). Oxytocin was administered intravenously to stimulate milk let-down and an intramuscular prophylactic dose of tetracycline was given, as reported previously (Watson et al, 2020). Milks were frozen at -20 • C and stored at -20 to -25 • C until aliquoted for analysis.…”

“…It is required for a wide range of synthetic processes such as for amino acids, carbohydrates, lipids, and heme, the pups' need for all of which may arise later during growth and development. We had previously found that the serum of seal pups accumulates higher concentrations of pyridoxine than are present in their mothers, leading to the suggestion that pups accumulate a stockpile of this metabolite to satisfy a dependency on it during their subsequent long fast (Figure 3; Watson et al, 2020).…”

“…For pyridoxine, the levels in both milk (note the scale break) and mother and pup serum are given; for serum data see ref. Watson et al (2020). See Supplementary A Figure S3 for comparison with cow and goat milks.…”

Energetic limits: Defining the bounds and trade‐offs of successful energy management in a capital breeder

“…by investigating metabolite trends leading up to weaning; Mellish & Iverson, 2001;Watson, Pomeroy, Al-Tannak, & Kennedy, 2020).…”