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

Oldřich Tomášek,Michal Vinkler,Barbora Gabrielová,Kamila Syslová,Tomáš Albrecht,Jana Svobodová,Petr Maršík,Petr Kačer

doi:10.1038/srep23546

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.

Highlights

Antioxidant function, proposing instead that redox homeostasis is signalled through Reactive oxygen and nitrogen species (ROS)-induced carotenoid oxidation and cleavage, which results in colour loss that can be prevented by an efficient antioxidant system[12]
Since a change in oxidative stress intensity can be manifested as either a change in oxidative damage or in antioxidant activity[29], we predict that carotenoid supplementation will result in (a) a reduction in oxidative damage and/or activity of antioxidants other than carotenoids due to their reduced need[18,29,30,31] if carotenoids act as antioxidants, (b) an increase in either one or both of these parameters if carotenoids act as pro-oxidants, or (c) no effect on either parameter if carotenoids have no influence on redox homeostasis
Using a novel measure of lipophilic antioxidant capacity, we demonstrate that carotenoids are able greatly inhibit the effect of oxidative challenge on redox state, thereby supporting the recently questioned antioxidant function of carotenoids in vivo

Summary

Introduction

Antioxidant function, proposing instead that redox homeostasis is signalled through ROS-induced carotenoid oxidation and cleavage, which results in colour loss that can be prevented by an efficient antioxidant system[12]. An extension of this hypothesis is the ‘handicap hypothesis’, which proposes that high levels of carotenoids may directly aggravate oxidative stress through pro-oxidant activity of carotenoid cleavage products, thereby posing a direct physiological handicap[15,16]. Most commonly-used antioxidant assays (e.g. FRAP, ORAC, OXY-Adsorbent test, TEAC or TRAP), measure antioxidant capacity in aqueous media only, which renders them unsuitable for evaluation of lipophilic antioxidants such as carotenoids[19,20]. Since a change in oxidative stress intensity can be manifested as either a change in oxidative damage or in antioxidant activity (or, both together)[29], we predict that carotenoid supplementation will result in (a) a reduction in oxidative damage and/or activity of antioxidants other than carotenoids due to their reduced need[18,29,30,31] (lowered ZE/tHODE ratio) if carotenoids act as antioxidants, (b) an increase in either one or both of these parameters if carotenoids act as pro-oxidants, or (c) no effect on either parameter if carotenoids have no influence on redox homeostasis

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