Extrinsic Versus Intrinsic Control of Avian Communication Based on Colorful Plumage Porphyrins

Abstract

Studies of avian visual communication are often approached from the perspective of adaptation-based hypotheses couched in an ecological framework. Despite their exceptional ecological diversity, however, birds express relatively few pigment categories in their visual signals or receptors. The mismatch between ecologic and pigment diversity suggests the operation of non-ecological constraints on avian visual communication. Colorful plumage porphyrins (turacoverdin and turacin) were examined to determine if both signal and receptor pigment absorption patterns co-vary with ecology, if only plumage pigment absorption varies with ecology, or if plumage and receptor pigment absorption are tied to each other’s physicochemical, physiological, and phylogenetic characteristics rather than to ecology. Physicochemical constraints on signal form were suggested by the persistence of the plumage pigments’ diagnostic spectral structure across lineages despite dramatic ecological differences. Physiological constraints on communication were suggested by the occurrence of colorful porphyrins only in birds with violet-sensitive (VS) vision, whose receptor sensitivities aligned to colorful porphyrin spectral structure much more strongly than did receptors of alternative visual systems. Phylogenetic constraints on these associations were evidenced by restriction of colorful plumage porphyrins to just a few lineages, all non-passerines (galliforms, musophagiforms, and charadriiforms). Synthesis of these patterns indicated that VS visual systems always evolved prior to colorful plumage porphyrins, suggesting a sensory bias for plumage pigments based on signal-receptor alignment. Patterns for colorful porphyrins and violet-sensitive systems reinforce the functional coupling between signal and receptor pigments observed for carotenoid plumage pigments in ultraviolet-sensitive birds, but the pairings differ in details of their alignments.