Could alternative pathways for carotenoid transformation affect colour production efficiency? A correlative study in wild common crossbills (Loxia curvirostra)

In many vertebrates, dietary yellow carotenoids are enzymatically transformed into 4C-ketocarotenoid pigments, leading to conspicuous red colourations. These colourations may evolve as signals of individual quality under sexual selection. To evolve as signals, they must transmit reliable information benefiting both the receiver and the signaler. Some argue that the reliability of 4C-ketocarotenoid-based colourations is ensured by the tight link between individual quality and mitochondrial metabolism, which is supposedly involved in transforming yellow carotenoids. We studied how a range of carotenoids covary in the feathers and blood plasma of a large number (n > 140) of wild male common crossbills (Loxia curvirostra). Plumage redness was mainly due to 3-hydroxy-echinenone (3HOE). Two other, less abundant, red 4C-ketocarotenoids (astaxanthin and canthaxanthin) could have contributed to feather colour as they are redder pigments. This was demonstrated for astaxanthin but not canthaxanthin, whose feather levels were clearly uncorrelated to colouration. Moreover, moulting crossbills carried more 3HOE and astaxanthin in blood than non-moulting ones, whereas canthaxanthin did not differ. Canthaxanthin and 3HOE can be formed from echinenone, a probable product of dietary β-carotene ketolation. Echinenone could thus be ketolated or hydroxylated to produce canthaxanthin or 3HOE, respectively. In moulting birds, 3HOE blood levels positively correlated to astaxanthin, its product, but negatively to canthaxanthin levels. Redder crossbills also had lower plasma canthaxanthin values. A decrease in hydroxylation relative to ketolation could explain canthaxanthin production. We hypothesize that red colouration could indicate birds' ability to avoid inefficient deviations within the complex enzymatic pathways.