Opposing effects of oxidative challenge and carotenoids on antioxidant status and condition-dependent sexual signalling

Abstract

Several recent hypotheses consider oxidative stress to be a primary constraint ensuring honesty of condition-dependent carotenoid-based signalling. The key testable difference between these hypotheses is the assumed importance of carotenoids for redox homeostasis, with carotenoids being either antioxidant, pro-oxidant or unimportant. We tested the role of carotenoids in redox balance and sexual signalling by exposing adult male zebra finches (Taeniopygia guttata) to oxidative challenge (diquat dibromide) and manipulating carotenoid intake. As the current controversy over the importance of carotenoids as antioxidants could stem from the hydrophilic basis of commonly-used antioxidant assays, we used the novel measure of in vivo lipophilic antioxidant capacity. Oxidative challenge reduced beak pigmentation but elicited an increase in antioxidant capacity suggesting resource reallocation from signalling to redox homeostasis. Carotenoids counteracted the effect of oxidative challenge on lipophilic (but not hydrophilic) antioxidant capacity, thereby supporting carotenoid antioxidant function in vivo. This is inconsistent with hypotheses proposing that signalling honesty is maintained through either ROS-induced carotenoid degradation or the pro-oxidant effect of high levels of carotenoid-cleavage products acting as a physiological handicap. Our data further suggest that assessment of lipophilic antioxidant capacity is necessary to fully understand the role of redox processes in ecology and evolution.

Figure 1. Effects of oxidative load and carotenoid intake on beak colouration, circulating carotenoids, body mass and blood redox state.

Birds were exposed to either low (ROS−) or high oxidative load (ROS+) and to either low (CAR−) or high carotenoid intake (CAR+). Bars represent group means controlled for pre-experimental values and their standard errors obtained from the models in Table 1. Shown are model P-values for the main effects of oxidative challenge (ROS) and carotenoid intake (CAR), as well as their interaction (INT). (a,b) Both, beak red chroma (higher values = more saturated red colour) and total plasma carotenoids were reduced by oxidative challenge and enhanced by high carotenoid intake. (c) Neither treatment factor had a significant effect on body mass, though their interaction resulted in body mass in ROS + CAR + group that was lower than would be expected if both effects were additive. None of the treatment groups, however, differed from the control (Tukey’s post-hoc test on change scores: P ≥ 0.379). (d–f) Oxidative challenge elicited a marked increase in both, lipophilic (ZE/tHODE) and hydrophilic (OXY) antioxidant capacity, resulting in marginally insignificant increase in blood oxidative damage (8-isoprostane). Carotenoids counteracted the effect of oxidative challenge on the activity of other lipophilic antioxidants (shown as reduced ZE/tHODE ratio) while having no effect on oxidative damage levels. On the other hand, hydrophilic antioxidant capacity was unaffected by lipophilic carotenoids.