Fitness correlates of blubber oxidative stress and cellular defences in grey seals (Halichoerus grypus): support for the life-history-oxidative stress theory from an animal model of simultaneous lactation and fasting

Abstract

Life-history-oxidative stress theory predicts that elevated energy costs during reproduction reduce allocation to defences and increase cellular stress, with fitness consequences, particularly when resources are limited. As capital breeders, grey seals are a natural system in which to test this theory. We investigated oxidative damage (malondialdehyde (MDA) concentration) and cellular defences (relative mRNA abundance of heat shock proteins (Hsps) and redox enzymes (REs)) in blubber of wild female grey seals during the lactation fast (n = 17) and summer foraging (n = 13). Transcript abundance of Hsc70 increased, and Nox4, a pro-oxidant enzyme, decreased throughout lactation. Foraging females had higher mRNA abundance of some Hsps and lower RE transcript abundance and MDA concentrations, suggesting they experienced lower oxidative stress than lactating mothers, which diverted resources into pup rearing at the expense of blubber tissue damage. Lactation duration and maternal mass loss rate were both positively related to pup weaning mass. Pups whose mothers had higher blubber glutathione-S-transferase (GST) expression at early lactation gained mass more slowly. Higher glutathione peroxidase (GPx) and lower catalase (CAT) were associated with longer lactation but reduced maternal transfer efficiency and lower pup weaning mass. Cellular stress, and the ability to mount effective cellular defences, could proscribe lactation strategy in grey seal mothers and thus affect pup survival probability. These data support the life-history-oxidative stress hypothesis in a capital breeding mammal and suggest lactation is a period of heightened vulnerability to environmental factors that exacerbate cellular stress. Fitness consequences of stress may thus be accentuated during periods of rapid environmental change.

Keywords: Adipose; Cellular chaperone; Cellular stress; Pinniped; Trade off.

Fig. 1

Change in relative mRNA abundance (calculated as ΔC_T) of a Nox4 (n = 17; all females) and b Hsc70 (n = 14; outlier females removed) between early and late lactation in grey seal mothers. Boxes represent interquartile range (IQR), horizontal bar represents median, whiskers represent 1.5 times IQR and points represent outliers. Asterisk indicates significantly lower or higher values

Fig. 2

Principle component (PC) scores of relative mRNA abundance (calculated as ΔC_T) of a Hsps and b REs in female grey seals at early lactation (black, open circle; lactating-fasting mothers; n = 17) and during the summer foraging period (blue, closed triangle; foraging (presumed pregnant) females; n = 13). All females were included. Percentage of total variance explained by the two principal components is indicated (%)

Fig. 3

Difference in MDA concentrations (nmol µL⁻¹) between foraging (presumed pregnant; n = 12) and lactating-fasting (n = 16) female grey seals. Boxes represent interquartile range (IQR), horizontal bar represents median, whiskers represent 1.5 times IQR and points represent outliers. Asterisk indicates significantly different values (t-test; p < 0.05)