A mitochondria-targeted antioxidant affects the carotenoid-based plumage of red crossbills

ABSTRACT The mechanisms involved in the production of red carotenoid-based ornaments in vertebrates are still poorly understood. Those colours generated by red carotenoids often depend on the enzymatic production (ketolation) of these pigments from dietary yellow carotenoids. Recently, it has been proposed that this conversion takes place at the inner mitochondrial membrane (IMM). This implies that carotenoid ketolation and cell respiration could share the same biochemical pathways. Such a link would favour the evolution of red ketocarotenoid-based ornaments as reliable indices of individual quality under a sexual selection scenario. We exposed captive male red crossbills ( Loxia curvirostra Linnaeus) to two different synthetic antioxidants designed to penetrate into the IMM: a synthetic ubiquinone (mitoQ) and a superoxide dismutase mimetic (mitoTEMPO). MitoQ decreased the blood levels of substrate yellow carotenoids and tocopherol. This could be attributed to the characteristics of the mitoQ molecule, which can distort the IMM structure, increasing free radical (superoxide) production and, potentially, antioxidant consumption. Contrarily, mitoTEMPO-treated birds increased the plasma levels of the second most abundant red ketocarotenoid of red crossbills (i.e. canthaxanthin). MitoTEMPO also increased plumage redness and total ketocarotenoid concentration in feathers among those birds exhibiting a redder plumage at the beginning of the study, rising the plasma values of the main red pigment (3-hydroxyechinenone) in paler birds. The results as a whole support the involvement of the mitochondrial antioxidant machinery in carotenoid biotransformation. The fact that the initial plumage redness determined the effect of mitoTEMPO suggests that the mitochondrial-based mechanism is intimately linked to individual quality. Summary statement Antioxidants designed to penetrate the mitochondrial membrane increased avian plumage redness but depending on pre-existing colouration. This supports mitochondrial involvement in the evolution of carotenoid-based ornaments as reliable quality signals.