History and mechanisms of carotenoid plumage evolution in the New World orioles (Icterus)

While many recent studies focus on the functions of carotenoids in visual signaling, they seldom address the phylogenetic origins of plumage coloration and its mechanisms. Here, we used the New World orioles (Icterus) as a model clade to study the history of orange carotenoid-based coloration and pigmentation, sampling 47 museum specimens from 12 species. We examined the identity and concentration of carotenoids in oriole feathers using high-performance liquid chromatography, and used phylogenetic comparative methods to compare these observations to reflectance measurements of plumage. Each of the seven yellow oriole species we sampled used only lutein to color their feathers. Ancestral state reconstruction of this trait suggests that the oriole common ancestor had yellow feathers pigmented with lutein. We found keto-carotenoids in small concentrations in the plumage of each of the five species scored as orange. This correlation suggests that discrete gains and losses of keto-carotenoids are behind independent gains of orange coloration in orioles. In contrast, total carotenoid concentration was not associated with hue, and total concentration of keto-carotenoids poorly explained variation in hue among species where they were present. These findings suggest that orioles most likely evolved orange plumage coloration at least twice, each time by gaining the ability to metabolize dietary carotenoids by C4-oxygenation. Given that red coloration is generated by this same oxygenation process in a wide range of bird species, it raises the question of why, if orioles possess this metabolic capability, no red oriole species exist.