Rapid changes in Atlantic grey seal milk from birth to weaning – immune factors and indicators of metabolic strain

Abstract

True seals have the shortest lactation periods of any group of placental mammal. Most are capital breeders that undergo short, intense lactations, during which they fast while transferring substantial proportions of their body reserves to their pups, which they then abruptly wean. Milk was collected from Atlantic grey seals (Halichoerus grypus) periodically from birth until near weaning. Milk protein profiles matured within 24 hours or less, indicating the most rapid transition from colostrum to mature phase lactation yet observed. There was an unexpected persistence of immunoglobulin G almost until weaning, potentially indicating prolonged trans-intestinal transfer of IgG. Among components of innate immune protection were found fucosyllactose and siallylactose that are thought to impede colonisation by pathogens and encourage an appropriate milk-digestive and protective gut microbiome. These oligosaccharides decreased from early lactation to almost undetectable levels by weaning. Taurine levels were initially high, then fell, possibly indicative of taurine dependency in seals, and progressive depletion of maternal reserves. Metabolites that signal changes in the mother’s metabolism of fats, such as nicotinamide and derivatives, rose from virtual absence, and acetylcarnitines fell. It is therefore possible that indicators of maternal metabolic strain exist that signal the imminence of weaning.

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

“…We had found before that levels of taurine decline steadily with time after birth in grey seal milk (Lowe et al, 2017), and this is even clearer in the current analysis (Figure 3). Carnivory provides a plentiful and continuous supply of taurine, which is known or suspected to be an essential dietary nutrient in some hypercarnivores (Hedberg et al, 2007(Hedberg et al, , 2011Chesney et al, 2009).…”

“…As with lactose, lacto-Ntetraose was present in day 2 seal milk samples and then virtually disappeared (Figure 2). We previously noted the presence and then rapid loss of defensive oligosaccharides such as sialyllactose and fucosyllactose in grey seal milk (Lowe et al, 2017), and we now find that this pattern is a common theme for several different species of complex saccharides (Supplementary A Figure S2). FIGURE 2 | Changes in levels of lactose and oligosaccharides of grey seal mothers' milks with time after parturition.…”

“…In Atlantic grey seals we previously reported that the change in milk from colostrum to mature phase lactation occurs faster than has been reported for any other group of mammals (Lowe et al, 2017). The rapidity of the effect was clearly apparent for proteins, but there were indications that the small molecule metabolome changed more slowly and that there were indicators of metabolic strain as the mothers' fasts progressed toward weaning (Lowe et al, 2017).…”

“…Milks were frozen at -20 • C and stored at -20 to -25 • C until aliquoted for analysis. Whole milk samples were used here, without removal of the fat layer, unlike in our previous report in which milk had been cold-centrifuged and the fat layer discarded (Lowe et al, 2017).…”

“…The gradient program was as follows: 80% B (0 min) 20% B (30 min) 5% B (36 min) 80% B (37 min) 80% B (45 min). Peak extraction and alignment were carried out by using MZMine 2.14 software, as previously described (Lowe et al, 2017). Metabolites were identified by searching against an in-house metabolite database in house data base drawn from the Human Metabolome Database 1 , KEGG 2 , and Lipid Maps 3 .…”