Sexual selection has resulted in a wide array of ornaments used in mate choice, and such indicator traits signal quality honestly when they bear costs, precluding cheating. Carotenoid-dependent coloration has attracted considerable attention in this context, because investing carotenoids in coloration has to be traded off against its physiological functions; carotenoids are antioxidants and increase immunocompetence. This trade-off is hypothesized to underlie the honesty of carotenoid-dependent coloration, signaling the “handicap” of allocating carotenoids away from somatic maintenance toward sexual display. Utilizing recent advances in modeling adaptive evolution, we used a comparative approach to investigate the evolution of plasma carotenoid levels using a species-level phylogeny of 178 bird species. We find that the evolutionary optimum for carotenoid levels is higher in lineages that evolved carotenoid-dependent coloration, with strong attraction toward this optimum. Hence, carotenoids do not appear to be limiting, given that higher carotenoid levels readily evolve in response to the evolution of carotenoid-dependent coloration. These findings challenge the assumption that carotenoids are a scarce resource and thus also challenge the hypothesis that physiological resource value of carotenoids underlies honesty of carotenoid-dependent traits. Therefore, the comparative evidence suggests that other factors, such as the acquisition and incorporation of carotenoids, are involved in maintaining signal honesty.