Predictive and reactive changes in antioxidant defence system in a heterothermic rodent

Abstract

Living in a seasonal environment requires periodic changes in animal physiology, morphology and behaviour. Winter phenotype of small mammals living in Temperate and Boreal Zones may differ considerably from summer one in multiple traits that enhance energy conservation or diminish energy loss. However, there is a considerable variation in the development of winter phenotype among individuals in a population and some, representing the non-responding phenotype (non-responders), are insensitive to shortening days and maintain summer phenotype throughout a year. Differences in energy management associated with the development of different winter phenotypes should be accompanied by changes in antioxidant defence capacity, leading to effective protection against oxidative stress resulting from increased heat production in winter. To test it, we analysed correlation of winter phenotypes of Siberian hamsters (Phodopus sungorus) with facultative non-shivering thermogenesis capacity (NST) and oxidative status. We found that in both phenotypes acclimation to winter-like conditions increased NST capacity and improved antioxidant defence resulting in lower oxidative stress (OS) than in summer, and females had always lower OS than males. Although NST capacity did not correlate with the intensity of OS, shortly after NST induction responders had lower OS than non-responders suggesting more effective mechanisms protecting from detrimental effects of reactive oxygen metabolites generated during rewarming from torpor. We suggest that seasonal increase in antioxidant defence is programmed endogenously to predictively prevent oxidative stress in winter. At the same time reactive upregulation of antioxidant defence protects against reactive oxygen species generated during NST itself. It suggests that evolution of winter phenotype with potentially harmful characteristics was counterbalanced by the development of protective mechanisms allowing for the maintenance of phenotypic adjustments to seasonally changing environment.

Keywords: Antioxidant defence; Heat production; Non-shivering thermogenesis; Oxidative stress; Photoresponsiveness; Polymorphism; Seasonal adjustments; Winter phenotype.

Photo 1

Different winter phenotypes frequently occur in the same litter. These photographs, taken with thermal camera (FLIR T540), show siblings from our colony kept under SP and T_a of 20 °C, one of which is non-responder (grey fur, on the left) and the other is responder (whitening, on the right). While taking photographs, non-responder was active while responder was torpid

Fig. 1

Body mass (g) of responding and nonresponding Siberian hamsters in summer (white boxes) and winter (grey boxes). Box indicates 25th and 75th percentiles, solid line stands for median and dots are outliers

Fig. 2

Reactive oxygen metabolites (ROM; mgH₂O₂ dL⁻¹, a), biological antioxidant potential (BAP mmol vit C L⁻¹, b) and oxidative stress (ROM/BAP, c) in summer- (white boxes) and winter-acclimated (grey boxes) male and female Siberian hamsters. Box indicates 25th and 75th percentiles, solid line stands for median and dots are outliers

Fig. 3

Relation between non-shivering thermogenesis capacity (NST, W) and body mass (g) in responding (upper panel) and non-responding (lower panel) Siberian hamsters acclimated to summer (white symbols, dashed regression lines) and winter conditions (grey symbols, solid regression lines)

Fig. 4

Mass-specific non-shivering thermogenesis (NST, W g⁻¹) in summer- (white boxes) and winter-acclimated (grey boxes) male and female Siberian hamsters, non-responding and responding to short photoperiod. Box indicates 25th and 75th percentiles, solid line stands for median and dots are outliers

Fig. 5

Relationship between Reactive Oxygen Metabolites (ROM, mg H₂O₂ dL⁻¹; a), Biological Antioxidant Potential (BAP, mmol vit C L⁻¹; b) and residual NST (W) in hamsters (n = 42) responding to seasonal changes in photoperiod (grey symbols) and not responding to seasonal changes (white symbols)

Fig. 6

Reactive oxygen metabolites (ROM, mg H₂O₂ dL⁻¹) and biological antioxidant potential (BAP, mmol vit C L⁻¹) following NST induction with noradrenaline in Siberian hamsters (n = 42) responding (grey symbols) and non-responding (white symbols) to seasonal changes in photoperiod. Large points indicate mean and whiskers indicate 95% confidence interval of the mean

Fig. 7

Biological antioxidant potential (BAP, mmol vit C L⁻¹), reactive oxygen metabolites (ROM, mg H₂O₂ dL⁻¹) and oxidative stress (ROM/BAP) after induction of facultative non-shivering thermogenesis (NA-injection) and control injection of saline solution which were measured in the same individuals of Siberian hamsters (n = 19)