Do carotenoid-based sexual traits signal the availability of non-pigmentary antioxidants?

Abstract

Carotenoid-based signals are thought to be indicators of male quality because they must be obtained from the diet and might thus indicate the ability of individuals to gather high-quality food. However, carotenoids are also known to have important physiological functions as immunoenhancers and antioxidants, and, as such, carotenoid-based sexual traits have also been suggested to reflect the health and antioxidant status of their bearers. This last idea is based on the hypothesis that carotenoids that are allocated to sexual signals are no longer available for the detoxification system. Recently, this hypothesis has been challenged on the grounds that the antioxidant activity is not the main biological role of carotenoids. Instead, carotenoid-based sexual traits might signal the availability of other non-pigmentary antioxidant molecules that might protect carotenoids from free radical attacks and make them available for sexual advertisements. We tested this hypothesis in the zebra finch, a passerine species with a carotenoid-based signal: the colour of the bill. We simultaneously manipulated the availability of carotenoids and of a non-pigmentary antioxidant (melatonin) in the drinking water. If the antioxidant properties of melatonin protect carotenoids from oxidation, we predict that birds supplemented with melatonin should have redder bills than birds not supplemented with melatonin, and that birds supplemented with carotenoids and melatonin should have redder bills than birds supplemented with carotenoids alone. Our findings are in agreement with these predictions since carotenoid and melatonin supplementation had an additive effect on bill colour. To our knowledge this is the first experimental evidence that a non-pigmentary antioxidant enhances the expression of a carotenoid-based sexual trait.