Molecular diversity, metabolic transformation, and evolution of carotenoid feather pigments in cotingas (Aves: Cotingidae)
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Carotenoid pigments were extracted from 29 feather patches from 25 species of cotingas (Cotingidae) representing all lineages of the family with carotenoid plumage coloration. Using high-performance liquid chromatography (HPLC), mass spectrometry, chemical analysis, and 1H-NMR, 16 different carotenoid molecules were documented in the plumages of the cotinga family. These included common dietary xanthophylls (lutein and zeaxanthin), canary xanthophylls A and B, four well known and broadly distributed avian ketocarotenoids (canthaxanthin, astaxanthin, α-doradexanthin, and adonixanthin), rhodoxanthin, and seven 4-methoxy-ketocarotenoids. Methoxy-ketocarotenoids were found in 12 species within seven cotinga genera, including a new, previously undescribed molecule isolated from the Andean Cock-of-the-Rock Rupicola peruviana, 3′-hydroxy-3-methoxy-β,β-carotene-4-one, which we name rupicolin. The diversity of cotinga plumage carotenoid pigments is hypothesized to be derived via four metabolic pathways from lutein, zeaxanthin, β-cryptoxanthin, and β-carotene. All metabolic transformations within the four pathways can be described by six or seven different enzymatic reactions. Three of these reactions are shared among three precursor pathways and are responsible for eight different metabolically derived carotenoid molecules. The function of cotinga plumage carotenoid diversity was analyzed with reflectance spectrophotometry of plumage patches and a tetrahedral model of avian color visual perception. The evolutionary history of the origin of this diversity is analyzed phylogenetically. The color space analyses document that the evolutionarily derived metabolic modifications of dietary xanthophylls have resulted in the creation of distinctive orange-red and purple visual colors.
KeywordsPlumage coloration Color space modeling Phylogeny
The authors would like to thank Dr. Shanti Kaligotla-Ghosh for conducting the 1H-NMR analysis, and Dr. Dennis Hill of the UConn Biotechnology and Bioservices Center for carrying out the high-resolution mass spectrometry. We also thank Dr. Tomáš Polívka for providing the rhodoxanthin standard. ROP thanks the Ikerbasque Foundation and the Donostia International Physics Center for research support. HAF thanks the University of Connecticut Research Foundation. Feather specimens for the analysis and reflectance measurements were kindly provided by the Philadelphia Academy of Natural Sciences (ANSP), Yale Peabody Museum of Natural History (YPM), University of Kansas Natural History Museum (KU), and the American Museum of Natural History (AMNH), and to Nate Rice for specimen loan from the Philadelphia Academy of Natural Sciences. Thanks to Joel Cracraft, George Barrowclough, and Paul Sweet for facilitating our work at the American Museum. We thank Jeffery Townsend for helpful discussion of metabolic modeling, and three anonymous reviewers for comments on the manuscript. The research was supported by the Yale University W. R. Coe Fund. We kindly thank Nick Athanas, Tanguy Deville, and Ciro Albano for permission to reproduce their lovely images of the plumages of wild cotinga species.
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