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ABSTRACT The carotenoid‐based colours of birds are a celebrated example of biological diversity and an important system for the study of evolution. Recently, a two‐step mechanism, with the enzymes cytochrome P450 2J19 (CYP2J19) and 3‐hydroxybutyrate dehydrogenase 1‐like (BDH1L), was described for the biosynthesis of red ketocarotenoids from yellow dietary carotenoids in the retina and plumage of birds. A common assumption has been that all birds with ketocarotenoid‐based plumage coloration used this CYP2J19/BDH1L mechanism to produce red feathers. We tested this assumption in house finches (Haemorhous mexicanus) by examining the catalytic function of the house finch homologues of these enzymes and tracking their expression in birds growing new feathers. We found that CYP2J19 and BDH1L did not catalyse the production of 3‐hydroxy‐echinenone (3‐OH‐echinenone), the primary red plumage pigment of house finches, when provided with common dietary carotenoid substrates. Moreover, gene expression analyses revealed little to no expression ofCYP2J19in liver tissue or growing feather follicles, the putative sites of pigment metabolism in moulting house finches. Finally, although the hepatic mitochondria of house finches have high concentrations of 3‐OH‐echinenone, observations using fluorescent markers suggest that both CYP2J19 and BDH1L localise to the endomembrane system rather than the mitochondria. We propose that house finches and other birds that deposit 3‐OH‐echinenone as their primary red plumage pigment use an alternative enzymatic pathway to produce their characteristic red ketocarotenoid‐based coloration. 

Abstract In birds, the process of speciation is closely associated with transitions in ornamentation, including coloration, plumage pattern, and song. To investigate the origins of these shifts and their connection to genetic changes, we conducted a study on one of the most highly ornamented songbirds, the Painted Bunting (Passerina ciris). The male Painted Buntings exhibits a stunning array of colors, with a red chest, blue head, green back, green coverts, and pink rump. In addition, Painted Buntings show a high level of genetic structure, with eastern and western populations that have fixed genetic differences in both nuclear and mitochondrial genes. Using non-invasive spectrophotometry techniques, we measured the coloration of six plumage patches on 88 museum specimens of male Painted Buntings in definitive plumage from across the range of the species. We predicted that there would be divergence between the genetically distinct eastern and western populations in ornamental coloration that is perceptible to a bunting but imperceptible to a human observer. However, we measured no consistent nor substantial difference in the plumage coloration of males from different populations. The observation of substantial divergence in nuclear and mitochondrial genotype with no change in ornamental coloration between populations of a brightly colored bird has important implications for the role of sexual selection in the process of speciation. 

ABSTRACT Even as numerous studies have documented that the red and yellow coloration resulting from the deposition of carotenoids serves as an honest signal of condition, the evolution of condition dependency is contentious. The resource trade‐off hypothesis proposes that condition‐dependent honest signalling relies on a trade‐off of resources between ornamental display and body maintenance. By this model, condition dependency can evolve through selection for a re‐allocation of resources to promote ornament expression. By contrast, the index hypothesis proposes that selection focuses mate choice on carotenoid coloration that is inherently condition dependent because production of such coloration is inexorably tied to vital cellular processes. These hypotheses for the origins of condition dependency make strongly contrasting and testable predictions about ornamental traits. To assess these two models, we review the mechanisms of production of carotenoids, patterns of condition dependency involving different classes of carotenoids, and patterns of behavioural responses to carotenoid coloration. We review evidence that traits can be condition dependent without the influence of sexual selection and that novel traits can show condition‐dependent expression as soon as they appear in a population, without the possibility of sexual selection. We conclude by highlighting new opportunities for studying condition‐dependent signalling made possible by genetic manipulation and expression of ornamental traits in synthetic biological systems. 

Carotenoid-based coloration is an essential feature of avian diversity and has important roles in communication and mate choice. The red feathers of birds from phylogenetically diverse orders and families are pigmented with C4-ketocarotenoids produced via the successive action of Cytochrome P450 2 J19 (CYP2J19) and 3-hydroxybutyrate dehydrogenase 1-like (BDH1L) on yellow dietary precursors. Yet, the biochemistry of these enzymes remains incompletely understood. Here we present a series of experiments characterizing the substrates, intermediates, and products of CYP2J19 and BDH1L expressed in heterologous cell culture. We confirm that CYP2J19 preferentially hydroxylates the 4 and 4′ positions of β-ring substrates, but can also hydroxylate the 3 and 3′ positions of C4-ketocarotenoids. We confirm that BDH1L catalyzes the conversion of zeaxanthin to canary xanthophyll B (ε,ε’-carotene-3,3′-dione) a major pigment in plumage of many yellow bird species. These results suggest that the actions of CYP2J19 and/or BDH1L can explain the presence of many metabolically transformed carotenoids in avian tissues. 

In a hybrid zone between two tropical lekking birds, yellow male plumage of one species has introgressed asymmetrically replacing white plumage of another via sexual selection. Here, we present a detailed analysis of the plumage trait to uncover its physical and genetic bases and trace its evolutionary history. We determine that the carotenoid lutein underlies the yellow phenotype and describe microstructural feather features likely to enhance color appearance. These same features reduce predicted water shedding capacity of feathers, a potential liability in the tropics. Through genome-scale DNA sequencing of hybrids and each species in the genus, we identifyBCO2as the major gene responsible for the color polymorphism. TheBCO2gene tree and genome-wide allele frequency patterns suggest that carotenoid-pigmented collars initially arose in a third species and reached the hybrid zone through historical gene flow. Complex interplay between sexual selection and hybridization has thus shaped phenotypes of these species, where conspicuous sexual traits are key to male reproductive success. 

In many species of animals, red carotenoid-based coloration is produced by metabolizing yellow dietary pigments, and this red ornamentation can be an honest signal of individual quality. However, the physiological basis for associations between organism function and the metabolism of red ornamental carotenoids from yellow dietary carotenoids remains uncertain. A recent hypothesis posits that carotenoid metabolism depends on mitochondrial performance, with diminished red coloration resulting from altered mitochondrial aerobic respiration. To test for an association between mitochondrial respiration and red carotenoids, we held wild-caught, molting male house finches in either small bird cages or large flight cages to create environmental challenges during the period when red ornamental coloration is produced. We predicted that small cages would present a less favorable environment than large flight cages and that captivity itself would decrease both mitochondrial performance and the abundance of red carotenoids compared to free-living birds. We found that captive-held birds circulated fewer red carotenoids, showed increased mitochondrial respiratory rates, and had lower complex II respiratory control ratios—a metric associated with mitochondrial efficiency—compared to free-living birds, though we did not detect a difference in the effects of small cages versus large cages. Among captive individuals, the birds that circulated the highest concentrations of red carotenoids had the highest mitochondrial respiratory control ratio for complex II substrate. These data support the hypothesis that the metabolism of red carotenoid pigments is linked to mitochondrial aerobic respiration in the house finch, but the mechanisms for this association remain to be established.