Variation in carotenoid–protein interaction in bird feathers produces novel plumage coloration

Abstract

Light absorption by carotenoids is known to vary substantially with the shape or conformation of the pigment molecule induced by the molecular environment, but the role of interactions between carotenoid pigments and the proteins to which they are bound, and the resulting impact on organismal coloration, remain unclear. Here, we present a spectroscopic investigation of feathers from the brilliant red scarlet ibis (Eudocimus ruber, Threskiornithidae), the orangered summer tanager (Piranga rubra, Cardinalidae) and the violet-purple feathers of the white-browed purpletuft (Iodopleura isabellae, Tityridae). Despite their striking differences in colour, all three of these feathers contain canthaxanthin (b,b-carotene-4,4 0 -dione) as their primary pigment. Reflectance and resonance Raman (rR) spectroscopy were used to investigate the induced molecular structural changes and carotenoid-protein interactions responsible for the different coloration in these plumage samples. The results demonstrate a significant variation between species in the peak frequency of the strong ethylenic vibration (n 1 ) peak in the rR spectra, the most significant of which is found in I. isabellae feathers and is correlated with a red-shift in canthaxanthin absorption that results in violet reflectance. Neither polarizability of the protein environment nor planarization of the molecule upon binding can entirely account for the full extent of the colour shift. Therefore, we suggest that head-to-tail molecular alignment (i.e. J-aggregation) of the protein-bound carotenoid molecules is an additional factor.

Evolution of Carotenoid Pigmentation in Caciques and Meadowlarks (Icteridae): Repeated Gains of Red Plumage Coloration by Carotenoid C4-Oxygenation

“…Birds must produce plumage coloration using only those carotenoid compounds that are found in the diet, either directly or as precursors. If these dietary carotenoids are metabolically modified, only a limited number of modifications is possible that change carotenoid absorptive properties (Britton ; but see Mendes‐Pinto et al ). Thus carotenoid hue might be thought of as a bounded, discrete character that can easily be switched back and forth between yellow and red with the gain or loss of particular enzymes or their expression.…”

Evolutionary innovation and diversification of carotenoid‐based pigmentation in finches

“…Even among carotenoidpigmented birds, however, the identity and metabolic modification of particular plumage colorants only tell part of the story. For example, the same pigment (canthaxanthin) can produce red, redorange, and even purple plumage in different species, depending on molecular alignment and interaction with proteins (Mendes-Pinto et al 2012). Similarly, two species in the present study (Serinus pusillus and Carduelis carduelis) rely exclusively on modified yellow pigments to produce red plumage, demonstrating a rare evolutionary pathway to achieve red feathers within this taxon (though this phenomenon has previously been described for red-shouldered widowbirds Euplectes axillaris; Andersson et al 2007).…”

Vibrational spectroscopic analyses of unique yellow feather pigments (spheniscins) in penguins

“…Raman and mid-infrared spectroscopies are versatile methods for analysing chemical composition and molecular structure. Notably, Veronelli et al [35] determined chemical characteristics of psittacofulvins from a Raman spectroscopic study comparing parrot feather pigments and carotenoids, and Mendes-Pinto recently used Raman spectral information to link feather coloration with carotenoid-contortion [36]. Previous studies of spheniscin pigments have identified chromatic, chromatographic retention-time and solubility properties [17].…”