Evolutionary and physiological processes involved in carotenoid coloration in animals
Type of DegreePhD Dissertation
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Colorful animal ornaments have been a core research focus of the field of sexual selection in evolutionary biology, and carotenoid-based coloration has been particularly well-studied. Animals as diverse as fish, reptiles, and birds, have co-opted carotenoids from their potential physiological roles for use as colorants of conspicuous yellow, orange, and red sexual ornaments. Nearly 40 years of research has revealed a striking pattern in which animals sometimes prefer to mate with individuals with the most richly colored carotenoid-based ornament because they tend to be of higher quality than duller individuals of the same species. What is less clear however, is how variation in coloration between individuals is created. Here, I first discuss two hypotheses about the mechanisms that underlie variation in coloration of sexual ornaments within a species. I compare and contrast the costly signaling hypothesis, which posits that differential costs among high and low-quality individuals maintains honesty from colorful ornaments and the index signaling hypothesis, which states that color signals can be cost-free and honest when their production is intimately tied to core cellular process. Next, I present a test of the predictions of those hypotheses by examining patterns of condition-dependent signaling from carotenoids in the bird coloration literature using meta-analysis. Most coloration from carotenoids comes from two distinct pathways: animals either deposit carotenoids unmodified from their diet to the integument, or they metabolize dietary carotenoids though oxidation reactions to produce ketolated carotenoids used for coloration. I show that coloration derived from converted, but not dietary, carotenoids is tightly linked to measures of individual quality, suggesting that carotenoid conversion is an important factor in maintaining honesty from carotenoid-based ornaments. Despite the long history of carotenoid research, a vertebrate model system that is amenable to study the mechanistic basis for variation in carotenoid coloration and metabolism has not been identified. The biochemical processes of converting yellow dietary carotenoids to red carotenoids are conserved across taxa; from crustaceans to birds. Considering this conservation, I then propose a novel system for carotenoid physiology research, the red marine copepod Tigriopus californicus, and demonstrate that they convert dietary yellow carotenoids to the red carotenoid, astaxanthin. Next, using this copepod system, I test predictions of the hypothesis that mitochondrial function mediates the conversion of yellow carotenoids to red. I employ two methods to manipulate mitochondrial function: exogenous heavy metal exposure and hybridization. I demonstrate that modulation of aspects of mitochondria are associated with reduced accumulation of astaxanthin, which may be due to impairment of bioconverting yellow dietary carotenoids. Overall, my dissertation highlights key details about carotenoids used for coloration of sexual ornaments that have not been incorporated in hypotheses for the maintenance of honesty from colorful ornaments. Additionally, it describes a system that is amenable to experimental manipulations and is poised to answer decade’s old questions about the evolution of carotenoid coloration in animal ornaments.