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

David G Watson,Naser F Al-Tannak,Patrick P Pomeroy,Malcolm W Kennedy

doi:10.1038/s41598-020-64488-1

David G Watson, Naser F Al-Tannak + Show 2 more

Open Access

https://doi.org/10.1038/s41598-020-64488-1

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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.

Highlights

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
The true seals are unusual in that mothers in half of the species do not feed during lactation, during which time their pups may double their body weights[13,14,15,16,17], and mothers usually leave their offspring abruptly at weaning[8]
To distinguish systemic versus mammary sources of these compounds, and to better understand the significance of the observations in the milk metabolome for the mother and pup, we followed metabolomic changes in the peripheral blood of both mothers and pups from birth to weaning. We did this in Atlantic grey seals, Halichoerus grypus, whose females endure a fast while lactating for about twenty days before weaning their pups and returning to sea[8,16]

Summary

Introduction

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. At the extremes among eutherians are bears, which have altricial neonates and long lactations, to the many groups that have precocial offspring and shorter lactations relative to body size, such as the bovids and equids[4,7] It is the true seals (Phocidae) that exhibit the shortest (four days in hooded seals) and most intense lactations, with extremely rapid weight gain in their pups[8]. To distinguish systemic versus mammary sources of these compounds, and to better understand the significance of the observations in the milk metabolome for the mother and pup, we followed metabolomic changes in the peripheral blood of both mothers and pups from birth to weaning We did this in Atlantic grey seals, Halichoerus grypus, whose females endure a fast while lactating for about twenty days before weaning their pups and returning to sea[8,16]. How does a seal pup’s metabolism change from birth to weaning? How do pups prepare metabolically for their post-weaning fast on land? How does a mother seal’s metabolism alter during her fast? Are there discernible indicators of a mother reaching the point where her reserves are becoming depleted and she must return to feeding and abandon her pup?

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