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The Molecular Evolution of Rhodopsin in Marine-Derived

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The Molecular Evolution of Rhodopsin in Marine-Derived THE MOLECULAR EVOLUTION OF RHODOPSIN IN MARINE-DERIVED AND OTHER FRESHWATER FISHES by Alexander Van Nynatten A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Cell and Systems Biology University of Toronto © Copyright by Alexander Van Nynatten (2019) THE MOLECULAR EVOLUTION OF RHODOPSIN IN MARINE-DERIVED AND OTHER FRESHWATER FISHES A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Cell and Systems Biology University of Toronto © Copyright by Alexander Van Nynatten (2019) ABSTRACT Visual system evolution can be influenced by the spectral properties of light available in the environment. Variation in the dim-light specialized visual pigment rhodopsin is thought to result in functional shifts that optimize its sensitivity in relation to ambient spectral environments. Marine and freshwater environments have been shown to be characterized by different spectral properties and might be expected to place the spectral sensitivity of rhodopsin under different selection pressures. In Chapter two, I show that the rate ratio of non- synonymous to synonymous substitutions is significantly elevated in the rhodopsin gene of a South American clade of freshwater anchovies with marine ancestry. This signature of positive selection is not observed in the rhodopsin gene of the marine sister clade or in non-visual genes. ii In Chapter three I functionally characterize the effects of positively selected substitutions occurring on another independent invasion of freshwater made by ancestrally marine croakers. In vitro spectroscopic assays on ancestrally resurrected rhodopsin pigments reveal a red-shift in peak spectral sensitivity along the transitional branch, consistent with the wavelengths of light illuminating freshwater environments. Kinetics assays reveal that freshwater croaker rhodopsin might also possess more efficient dark adaptation. In Chapter four I use a comparative approach to show that substitutions with similar functional effects occur convergently during marine to freshwater transitions, but only in deeper-dwelling lineages. In Chapter five I investigate the molecular evolution of rhodopsin in Gymnotiformes, a clade of freshwater fishes with an alternative sensory modality specialized for dim-light environments. Rhodopsin is highly conserved in this clade, but bouts of positive selection are observed in association with ecological transitions, indicating that dim-light vision remains an important sensory modality in these freshwater fishes. Altogether, these studies show that shifts in selection pressures and substitutions that alter the functional properties of rhodopsin are frequently observed during ecological transitions into and within freshwater environments, as long as species inhabit depths where the attenuation of light is non-negligible. Furthermore, this thesis expands our understanding of the effects of ecology on visual evolution and its influence on the structural and functional properties of rhodopsin. iii ACKNOWLEDGMENTS This thesis would not have been possible without the help of many people. Most, if not all of the good ideas expressed within have benefited from bouncing off the brains of my family, friends and colleagues. I would first like to thank my supervisors, Nate and Belinda. They have not only provided me with a tremendous amount of support and guidance over the past six years but have also given me enough freedom to explore many of my own interests and ideas along with sending me to some truly remarkable and remote regions in the tropics. Their continued encouragement has been especially fundamental in my development as a writer and in fostering my passion in data visualization. I would also like to thank Jason Weir and Vince Tropepe for serving as my supervisory committee. They have helped shape this thesis into a coherent and feasible set of projects. I am grateful to John Calarco and David Liberles for donating their time to serve as my internal and external examiners respectively. My experience as a grad student was made so much more enjoyable thanks to my colleagues in the Chang and Lovejoy labs. I would especially like to thank Matt, Emma and JP for their help in the field. I may not have made it back from the tropics without them. However, the hospitality of Joe Waddell, Juan Bogota and JP's family made it a difficult decision to leave. I also owe a great deal of thanks to Gianni, Eduardo, James, Nihar and Ahmed in showing me the ropes with respect to many wet lab techniques, as well as showing a great deal of patience in this process. I would not have been able to make any sense of the data generated in the wet lab without bioinformatics help from Frances, Ben, Sarah, Dominik, Lujan, Ryan and Amir. I would also like to thank Devin Bloom for collecting most of the fishes I analyzed in this project. Finally, I would like to acknowledge all of the support I have received from all other past and present graduate and undergraduate students in both the Chang and Lovejoy labs. On top making me a better scientist, my lab mates have helped me develop into a better person and I consider myself very privileged to have had such a great bunch of people to learn from. iv I would also like to thank my family and friends. My parents, Kathy and Walter, are the hardest working people I know, but somehow have still always been there when I needed them. As much as I complained about having to milk cows, pick stones and stack hay, it has helped make me a more patient person and also provided some quality time to think. In addition to the tireless support I have received from my parents during my extended education, I was very fortunate to have supportive siblings, Nick and Evonne, and friends from back home in Perth County, London and Toronto. Finally, I owe a great deal of thanks to my best friend and partner Rowshyra. She has not only kept me motivated through the final stretch of this PhD process but has imbued in me deeper appreciation of what it takes to be a field biologist as well as a better understanding of the ecology of the fishes attached to the eyes that I study herein. v TABLE OF CONTENTS ACKNOWLEDGMENTS .................................................................................................................................. IV TABLE OF CONTENTS ................................................................................................................................... VI LIST OF TABLES .............................................................................................................................................. IX LIST OF FIGURES .............................................................................................................................................. X LIST OF ABBREVIATIONS ............................................................................................................................ XI CHAPTER ONE: GENERAL INTRODUCTION ............................................................................................ 1 1.1. THE EYE AND VISION ................................................................................................................................... 1 1.1.1. The evolution of the vertebrate eye ...................................................................................................... 1 1.1.2. Vertebrate eyes .................................................................................................................................... 2 1.1.3. Vertebrate retinas ............................................................................................................................... 3 1.1.4. The phototransduction cascade .......................................................................................................... 5 1.1.5. The retinoid cycle ................................................................................................................................ 6 1.2. VISUAL ECOLOGY ........................................................................................................................................ 7 1.2.1. Principles of light relevant to vision ................................................................................................... 7 1.2.2. The attenuation of light ....................................................................................................................... 8 1.2.3 Light underwater .................................................................................................................................. 9 1.3. THE EVOLUTION OF RHODOPSIN ................................................................................................................ 10 1.3.1. Opsin evolution ................................................................................................................................. 10 1.3.2. Opsin structure and function ............................................................................................................ 11 1.3.3. Differences in rod and cone opsin functional properties .................................................................. 12 1.3.4. Rhodopsin spectral tuning ................................................................................................................ 13 1.3.5 Mutations causing disease .................................................................................................................. 14 1.4. VISUAL EVOLUTION IN FISHES
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