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Molecular Evolution and Functional Characterization of the Visual Pigment Proteins of the Great Bowerbird (Chlamydera Nuchalis) and Other Vertebrates

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Molecular Evolution and Functional Characterization of the Visual Pigment Proteins of the Great Bowerbird (Chlamydera Nuchalis) and Other Vertebrates Molecular Evolution and Functional Characterization of the Visual Pigment Proteins of the Great Bowerbird (Chlamydera nuchalis) and Other Vertebrates by Ilke van Hazel A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Ilke van Hazel 2012 Molecular Evolution and Functional Characterization of the Visual Pigment Proteins of the Great Bowerbird (Chlamydera nuchalis) and Other Vertebrates Ilke van Hazel Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto 2012 Abstract Visual pigments are light sensitive receptors in the eye that form the basis of sensory visual transduction. This thesis presents three studies that explore visual pigment proteins in vertebrates using a number of computational and experimental methods in an evolutionary framework. The objective is not only to identify, but also to experimentally investigate the functional consequences of genetic variation in vertebrate visual pigments. The focus is on great bowerbirds (Chlamydera nuchalis), which are a model system in visual ecology due to their spectacular behaviour of building and decorating courtship bowers. There are 4 chapters: Chapter 1 introduces background information on visual pigments and vision in birds. Among visual pigment types, the short-wavelength-sensitive (SWS1) pigments have garnered particular interest due to the broad spectral range among vertebrates and the importance of UV signals in communication. Chapter 2 investigates the evolutionary history of SWS1 in vertebrates with a view toward its utility as a phylogenetic marker. Chapter 3 investigates SWS1 evolution and short-wavelength vision in birds, with particular focus on C. nuchalis and its SWS1. The evolution of spectral tuning mechanisms mediating UV/violet vision in passerines and parrots is elucidated in this chapter using site-directed mutagenesis, protein expression, and phylogenetic recreation of ancestral opsins. While cone opsins mediate colour vision in bright light, the rod ii visual pigment (RH1) contained in rod photoreceptors is critical for dim light vision. Detailed characterization of RH1 function has only been conducted on a few model systems. Chapter 4 examines C. nuchalis RH1 using a number of functional assays in addition to absorbance spectra, including hydroxylamine sensitivity and the rate of retinal release. This chapter includes an investigation into the role of amino acid mutations typical of dim-light adapted vertebrates, D83N and A292S, in regulating functional properties of bovine and avian RH1s using site- directed mutagenesis. Together these chapters describe naturally occurring mutations in visual pigments and explore the way they can influence visual perception. These represent one of the few investigations of visual pigments from a species that is not a model lab organism and form a significant contribution to the field of visual pigment biochemistry and evolution. iii Dedication This thesis is dedicated to My family. Thank you all for the love, support, encouragement and dedication. I have often had cause to feel that my hands are cleverer than my head. That is a crude way of characterizing the dialectics of experimentation. When it is going well, it is like a quiet conversation with Nature. One asks a question and gets an answer; then one asks the next question, and gets the next answer. An experiment is a device to make Nature speak intelligibly. After that one has only to listen. ~ George Wald 1968 iv Acknowledgments Throughout my studies I have received support and encouragement from a great number of individuals. It would not have been possible to write this thesis without the help of the kind people around me, to only some of whom it is possible to give mention here. Above all, I would like to thank Aaron. He has given unequivocal support, help and love for which I am forever grateful. My entire family has been a foundation through all the ups and downs of graduate school. I could not have done it without them. This thesis would not have been possible with out my principal supervisor, Belinda Chang. I would not be the academic I am today if it weren’t for her guidance. I’d also like to thank my dissertation committee of Drs. Allan Baker and David Guttman, for their advice, support and enthusiasm as I moved from an idea to a completed study. My thesis would also not be possible without the tissue samples provided by Drs. Lainy Day and John Endler. I am thankful for their generous donation. I would like to acknowledge the financial, academic and technical support of the University of Toronto, the Department of Ecology and Evolutionary Biology, the Ramsay Wright building and associated staff, for their support and assistance since the start of my graduate studies, especially head of the department, Dr. Nick Collins. The good advice, support and friendship of Drs. Helen Rodd and Steve Tobe have also been invaluable on both an academic and a personal level, for which I am extremely grateful. Amongst my fellow graduate students, I would especially like to thank Ekaterina Hult, Elisabeth Marchal, and Jenny Huang. Their support, help and friendship throughout the last stages of my thesis were most important. Also, I would be remiss to not acknowledge the friendship of Anna Price, Laura Timms, Jessica Ward, and Bonnie Fraser who made academic study, and especially coffee breaks, fun and friendly. I am most grateful to Cam Weadick for listening to my questions and digressions, as well as for providing patient guidance in molecular evolution. I am glad to have shared my PhD years with such a wonderfully intelligent and funny individual. In a similar vein, I am thankful to other members of the Chang lab, old and new, for their companionship and for opsin and science v discussions and I am especially thankful to those who helped me in the lab and reviewed my thesis chapters: James Morrow, David Yu, Shannon Refvik, Frances Hauser, Ryan Schott, Gianni Castiglione, Amir Sabouhanian, Benedict Darren, Jess Skillman, Natalie Chan, Jingjing Du, Clement Yang, Hermina Genu, Gloria Lin, Mengshu Xu, Savo Lazic, Francesco Santini, Conni Bickelmann, and Johannes Muller. Also, I extend thanks to Robert Pengelly, whose computer skills saved me many, many hours of work. I cannot find words to express my gratitude to Carmen Lia Murall, Amie Sergas, and Drs. Anne Kohler and Tara Moriarty whose friendship and faith in me as a fellow scientist and professional imparted the necessary confidence to succeed. Last, but by no means least, I thank my friends Monica Lavers, Meghan Whitfield, Andrea Marlowe, and Erin Eadie for their lasting friendship. I also thank the Dolls, current and former teammates- the most remarkable, supportive, and inspiring group of women anyone could ever meet. I would like to specifically mention; Kat Attack, Lucky, Iko, Santilly, Scarcasm, Dawson, Hoser, Bomber, Dolly Parts’em, Bonky, Lucid Lou, Sista, and Audrey, whose presence in my life has been particularly important. vi Table of Contents DEDICATION ........................................................................................................................................................... IV ACKNOWLEDGMENTS .......................................................................................................................................... V TABLE OF CONTENTS ........................................................................................................................................ VII LIST OF TABLES ..................................................................................................................................................... XI LIST OF FIGURES ................................................................................................................................................. XII LIST OF APPENDICES ........................................................................................................................................ XIV LIST OF ABBREVIATIONS ................................................................................................................................. XV CHAPTER 1 INTRODUCTION: VISUAL SYSTEM AS A MODEL FOR STUDYING ADAPTATION AND PROTEIN FUNCTION ............................................................................................................................................. 1 1 . ................................................................................................................................................................................................................................................................................................................... 1 1.1 INTRODUCTION: THE DIVERSITY IN VISUAL PIGMENT PROTEINS ........................................................................ 1 1.2 VISUAL PIGMENT STRUCTURE AND FUNCTION ........................................................................................................ 2 1.2.1 Rod photopigment structure .............................................................................................................................. 3 1.2.2 Retinal chromophore ............................................................................................................................................. 4 1.2.3 Phototransduction and the visual cycle .......................................................................................................
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