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Synopsis In many species of birds, red carotenoid coloration serves as an honest signal of individual quality, but the mechanisms that link carotenoid coloration to animal performance remain poorly understood. Most birds that display red carotenoid coloration of feathers, bills, or legs ingest yellow carotenoids and metabolically convert the yellow pigments to red. Here, we review two lines of investigation that have rapidly advanced understanding of the production of red carotenoid coloration in birds, potentially providing an explanation for how red coloration serves as a signal of quality: the identification of the genes that enable birds to be red and the confirmation of links between production of red pigments and core cellular function. CYP2J19 and BDH1L were identified as key enzymes that catalyze the conversion of yellow carotenoids to red carotenoids both in the retinas of birds for enhanced color vision and in the feathers and bills of birds for ornamentation. This CYP2J19 and BDH1L pathway was shown to be the mechanism for production of red coloration in diverse species of birds and turtles. In other studies, it was shown that male House Finches (Haemorhous mexicanus) have high concentrations of red carotenoids within liver mitochondria and that redness is positively associated with mitochondrial function. These observations suggested that the CYP2J19 and BDH1L pathway might be tightly associated with mitochondrial function. However, it was subsequently discovered that male House Finches do not use the CYP2J19 and BDH1L pathway to produce red pigments and that both CYP2J19 and BDH1L localize in the endoplasmic reticulum, not the mitochondria. Thus, we have the most detailed understanding of links between cellular function and redness in a bird species for which the enzymes to convert yellow to red pigments remain unknown, while we have the best understanding of the enzymatic pathways to red in species for which links to cellular function are largely unstudied. Deducing whether and how signals of quality arise from these distinct mechanisms of ornamental coloration is a current challenge for scientists interested in the evolution of honest signaling. 

Synopsis Sexual selection drives the evolution of a broad diversity of traits, such as the enlarged claws of fiddler crabs, the high-energy behavioral displays of hummingbirds, the bright red plumage of house finches, the elaborated antennae of moths, the wing “snapping” displays of manakins and the calculated calls of túngara frogs. A majority of work in sexual selection has aimed to measure the magnitude of these traits. Yet, we know surprisingly little about the physiology shaping such a diversity of sexually selected behavior and supportive morphology. The energetic properties underlying sexual signals are ultimately fueled by metabolic machinery at multiple scales, from mitochondrial properties and enzymatic activity to hormonal regulation and the modification of muscular and neural tissues. However, different organisms have different physiological constraints and face various ecological selection pressures; thus, selection operates and interacts at multiple scales to shape sexually selected traits and behavior. In this perspective piece, we describe illustrative case studies in different organisms to emphasize that understanding the physiological and energetic mechanisms that shape sexual traits may be critical to understanding their evolution and ramifications with ecological selection. We discuss (1) the way sexual selection shapes multiple integrated components of physiology, behavior, and morphology, (2) the way that sexually selected carotenoid pigments may reflect some aspects of cellular processes, (3) the relationship between sexually selected modalities and energetics, (4) the hormone ecdysone and its role in shaping sex-specific phenotypes in insects, (5) the way varied interaction patterns and social contexts select for signaling strategies that are responsive to social scenes, and (6) the role that sexual selection may have in the exploitation of novel thermal niches. Our major objective is to describe how sexually selected behavior, physiology, and ecology are shaped in diverse organisms so that we may develop a deeper and more integrated understanding of sexual trait evolution and its ecological consequences. 

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.