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Koch Dissertation.Pdf Exploring the role of carotenoid pigments in physiological function and color signals by Rebecca Elizabeth Koch A dissertation submitted to the Graduate Faculty of Auburn University in partial fulfillment of the requirements for the Degree of Doctor of Philosophy Auburn, Alabama May 7, 2017 Keywords: canary, carotenoid-based coloration, oxidative stress, immunocompetence, ornamentation, resource tradeoff hypothesis Copyright 2017 by Rebecca Elizabeth Koch Approved by Geoffrey E. Hill, Chair, Professor of Biology F. Stephen Dobson, Professor of Biology Gary Hepp, Professor Emeritus of Forestry and Wildlife Sciences Elizabeth H. Schwartz, Assistant Professor of Biology Abstract The study of carotenoid-based coloration, particularly in bird species, is a large and growing literature that is increasingly defined by the framework of a single overarching concept, the resource tradeoff hypothesis. Contrary to widespread acceptance of resource tradeoffs in maintaining the condition-dependence of carotenoid-colored signals, methodological and theoretical challenges alike have complicated my ability to conclusively test the hypothesis. Here, I first review the existing empirical literature that has attempted to test the resource tradeoff hypothesis in bird species, and I highlight outstanding uncertainty in several key components of the hypothesis as well as important directions for future research. Given that one of the primary complications in testing for differential resource allocation of carotenoid resources is the ability to experimentally manipulate dietary intake, I next present a meta- analysis that quantitatively describes the relationships between dietary carotenoid supplementation and changes to circulating carotenoid levels or carotenoid-based coloration. A second main complication in testing the resource tradeoff hypothesis is the ability to use experimental challenges to physiological systems to assess whether carotenoid pigments play a role in the response. While immune challenges, such as pathogen infection or parasite administration, have been better studied, experimental techniques that induce increased oxidative stress remain new and relatively unexplored; I therefore present the first comprehensive review of a variety of methods that have been or could potentially be used to induce increased oxidative stress in animal bodies without confounding side-effects. Before applying one of these ii techniques to my own study system, I first describe that system—the domestic canary (Serinus canaria)—in a short comparative study that uses feather samples and museum specimens to establish the evolution of sexual monochromatism through domestication. Finally, I perform my own empirical test of the core assumption of the resource tradeoff hypothesis, that carotenoid pigments provide direct physiological benefits, by examining whether carotenoid-free mutant canaries are unable to perform as well as carotenoid-rich wild-type canaries on immune and oxidative tests. The results of my analyses are a conclusive demonstration that birds do not need internal carotenoid pigments to defend against pathogens or prevent oxidative stress, at least when the confounding effects of retinol are removed. Collectively, my dissertation presents a critical examination of all angles of the resource tradeoff hypothesis, from reviewing existing evidence to raising methodological concerns to finally challenging the hypothesis with my own empirical study. My research offers an important advancement to understanding the role of carotenoid pigments in physiological processes in animals and to how future researchers study carotenoids, those physiological processes, and coloration itself. iii Acknowledgments Behind every scientist is an entire arsenal of support, from friends to family to mentors to coffee shop baristas. My advisor Dr. Geoff Hill and my unofficial mentor Dr. Wendy Hood have been absolutely tantamount to every of my successes over these past years; from personal to professional advice, I could always count on them—and often did—to help me find the way forward through the myriad challenges of live animal work. At the same time, my undergraduate mentor Dr. Gail Patricelli continues to shape the way I approach science, and life as a scientist. have measured my progress against their excellent examples, and I only hope that one day I can be as stellar a mentor to my own students. My labmates Maria, Dave, Roy, Molly, Ryan, Anna, and Matt have been there with me, and for me, for answers and support that only peers can give. Meanwhile, my colleagues at the Miller Writing Center—including my boss, Dr. James Truman—have been instrumental in keeping me sane through a balanced, open dialogue and friendships across disciplines and entirely separated from my work in Funchess Hall. Group fitness was similarly key to my sanity; instructors Christy, Lisa, Susannah, and Pam never fail to bring a smile (and a sweat) to my face, no matter how exhausted my mind or how dire my level of anxiety. More recently, Cheryl, Bennett, and the other fabulous Auburn Masters Swimmers have been an endless source of encouragement and balance as I dive headfirst (quite literally) into a sport from which I was certain I had retired, many years ago. I completed my written examinations in Mama Mocha’s—the local coffee shop—and I owe the friendly baristas and their delicious creations for a great deal of my productivity. At home, my fiancée David and my iv corgis Daisy and Colby keep me grounded in the unpredictable, maddening, and sometimes terrifying world of research; my parents, too, are always just a phone call away, no matter the hour and no matter the topic. Finally, I send a big thank you to my canaries. v Table of Contents Abstract ......................................................................................................................................... ii Acknowledgments........................................................................................................................ iv List of Tables ................................................................................................................................ x List of Figures .............................................................................................................................. xi Chapter 1 : Do carotenoid-based ornaments entail resource tradeoffs? An evaluation of theory and data ........................................................................................................................................ 1 Introduction ..................................................................................................................... 1 The Carotenoid Tradeoff Hypothesis................................................................................ 4 Are carotenoids limited? ....................................................................................... 5 Do carotenoids play important roles in immune and antioxidant function? ....... 8 Carotenoids as immune boosters .............................................................. 9 Rationale for the hypothesis.......................................................... 9 Case studies ................................................................................. 11 Conclusions ................................................................................. 15 Carotenoids as antioxidants .................................................................... 15 Rationale for the hypothesis........................................................ 15 Case studies ................................................................................. 16 Conclusions ................................................................................. 19 What makes a high quality individual? ............................................................... 20 Conclusions ................................................................................................................. 24 References ................................................................................................................. 26 vi Chapter 2 : The importance of carotenoid dose in supplementation studies with songbirds .... 35 Introduction ..................................................................................................................... 35 Methods........................................................................................................................... 38 Literature search.................................................................................................. 38 Carotenoid supplementation calculations ........................................................... 40 Effect size calculations ....................................................................................... 42 Statistical analyses .............................................................................................. 43 Results ............................................................................................................................. 45 Effect of carotenoid supplementation on plasma carotenoid levels.................... 45 Effect of carotenoid supplementation on coloration ........................................... 47 Publication bias ................................................................................................... 50 Discussion ....................................................................................................................... 50 Acknowledgments..........................................................................................................
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