Opposing effects on glutathione and reactive oxygen metabolites of sex, habitat, and spring date, but no effect of increased breeding density in great tits (Parus major)

Oxidative stress (i.e., more oxidants than antioxidants) has been proposed as a proximate currency in life-history trade-offs, which if studied in an ecological setting allow a more realistic perspective on the origin and evolution of trade-offs. Therefore, the aim here was to investigate the impact of ecological and individual factors for variation in markers of oxidative stress using both experimental and correlational data. Total glutathione (tGSH), oxidized glutathione (GSSG), plasma antioxidant capacity (OXY), and plasma-reactive oxygen metabolites (ROM) were measured in more than 700 breeding great tits (Parus major). The main results revealed a pronounced sex difference, with females having lower ROM and OXY, but higher tGSH compared with males. In addition, birds breeding in the evergreen areas had higher tGSH compared with those in the deciduous habitat, but the experimentally manipulated breeding density had no significant effect on any of the redox markers. Independent of the sex differences, the larger the reproductive investment the lower the ROM of both males and females. Taken together, the extracellular markers - ROM and OXY - revealed similar results and were highly correlated. Interestingly, the direction of their effects was in the opposite direction to the endogenously synthesized tGSH and GSSG. This highlights the need to combine extracellular markers with endogenously synthesized antioxidants to understand its implications for the origin and evolution of trade-offs in an ecological setting. Oxidative stress has been proposed as a proximate currency in life-history trade-offs, which if studied in an ecological setting allow a more realistic perspective on the origin and evolution of trade-offs. Here multiple markers of oxidative stress were analysed in wild great tits. The results reveal that the endogenously synthesized antioxidant glutathione and markers of plasma oxidative stress are affected in opposing directions with regard to sex, habitat type, and spring date. Clutch size was negatively associated with oxidative damage, which suggests that those with high reproductive investment can combat physiological costs linked to oxidative stress. The experimentally manipulated breeding density did not influence oxidative stress physiology. The study highlights the need to measure multiple markers to understand the role of oxidative stress in limiting the expression of life-history traits and trajectories in different ecological contexts.