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Coping with Life on Land: Physiological, Biochemical, and Structural Mechanisms to Enhance Function in Amphibious Fishes

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Coping with Life on Land: Physiological, Biochemical, and Structural Mechanisms to Enhance Function in Amphibious Fishes Coping with Life on Land: Physiological, Biochemical, and Structural Mechanisms to Enhance Function in Amphibious Fishes by Andy Joseph Turko A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Doctor of Philosophy in Integrative Biology Guelph, Ontario, Canada © Andy Joseph Turko, October 2018 ABSTRACT COPING WITH LIFE ON LAND: PHYSIOLOGICAL, BIOCHEMICAL, AND STRUCTURAL MECHANISMS TO ENHANCE FUNCTION IN AMPHIBIOUS FISHES Andy Joseph Turko Advisor: University of Guelph, 2018 Dr. Patricia A. Wright The invasion of land by fishes was one of the most dramatic transitions in the evolutionary history of vertebrates. In this thesis, I investigated how amphibious fishes cope with increased effective gravity and the inability to feed while out of water. In response to increased body weight on land (7 d), the gill skeleton of Kryptolebias marmoratus became stiffer, and I found increased abundance of many proteins typically associated with bone and cartilage growth in mammals. Conversely, there was no change in gill stiffness in the primitive ray-finned fish Polypterus senegalus after one week out of water, but after eight months the arches were significantly shorter and smaller. A similar pattern of gill reduction occurred during the tetrapod invasion of land, and my results suggest that genetic assimilation of gill plasticity could be an underlying mechanism. I also found proliferation of a gill inter-lamellar cell mass in P. senegalus out of water (7 d) that resembled gill remodelling in several other fishes, suggesting this may be an ancestral actinopterygian trait. Next, I tested the function of a calcified sheath that I discovered surrounding the gill filaments of >100 species of killifishes and some other percomorphs. I found no evidence that this calcification evolved to provide support in amphibious fish out of water. Instead, my experimental data suggests that the calcified sheath maintains the position of gill filaments during aquatic ventilation. The role of gill mechanics has largely been neglected in previous studies of respiratory function, but my data suggests that filament stiffness may be critically important. Finally, I tested the hypothesis that prolonged survival out of water is enabled by slow metabolism and conservation of energy stores in K. marmoratus, which cannot feed in air. I found that low metabolism prolonged survival out of water by almost two weeks and this phenotype had increased fecundity in microcosms that were intermittently dry for half of a year. There was no obvious trade-off in fully aquatic environments. Overall, this thesis integrates physiological, ecological, and evolutionary perspectives to provide new insight into how amphibious fishes survive out of water. ACKNOWLEDGEMENTS First and foremost, I want to thank my supervisor Dr. Pat Wright for all the wisdom she has shared over the past 10(!) years of working together. Pat – I can’t thank you enough for giving me my first opportunity in science as a naïve undergrad, and for the countless opportunities that have followed. You let me follow my interests wherever they led, and that has made my graduate experience more fulfilling than I could have ever hoped. I have learned so much from you about how to be a thoughtful, rigorous scientist, and about how to succeed in the modern scientific world. It has been an absolute privilege to work with you. Thank you so much to my committee members, Drs. Douglas Fudge, Todd Gillis, and Graham Scott, who were so helpful all along the way. My thesis was shaped in large part by your ideas, expertise, equipment, and experimental know-how. I appreciate all of our great discussions and look forward to many more. I have been lucky to work with fantastic collaborators each of my thesis chapters. To Drs. Frank Smith, Roger Croll, and Matt Stoyek – my time in Halifax was an all-time research highlight. Thank you so much for sharing your microgravity expertise for being so much fun to be around. Dr. Dietmar Kültz – thank you for conducting the gill proteomics analysis, your data made a huge contribution to my understanding of gill remodelling. To Dr. Em Standen – thank you for sharing your Polypterus expertise, for housing me in Ottawa, and for all the good times in Belize. Priyam Maini, I really appreciate all of our thoughtful discussions, and of course your attention to detail analyzing Polypterus gills. Drs. Trina Du and Javier Santos-Santos, thank you both also for your help interpreting micro-CT scans. Bianca Cisternino – you have impressed me so much over the years we have worked together. You were instrumental keeping the microcosms running on schedule, and I am indebted to you for all your hard work analyzing gill iv filament calcification. Dr. Ryan Earley - thank you for helping plan the microcosm experiments, the countless hours you spent analyzing microsatellites, and for all the stimulating conversations we have had over the years. You have taught me so much, and I look forward to learning more. Justine Doherty – working with you to understand emersion tolerance in rivulus has been both rewarding and fun. I really appreciate all of your insight, and of course your long hours in the lab measuring metabolic rate and energy stores. Irene Yin-Liao – thank you for your many, many contributions, it has been such fun to work alongside you. Kelly Levesque – your help designing and running the microcosms was invaluable, I really enjoyed working with you. Perryn Kruth – you are a master of gill dissection. Thank you so much for all your hard work. My co-conspirators in the Wright lab have been a major source of inspiration, knowledge, and good times. Dr. Chris Cooper, Hadi Dhiyebi, Kelly Regan, Mike Wells, Kristin Bianchini, Cayleih Robertson, Kelly Levesque, Quentin Heffel, Tessa Blanchard, Giulia Rossi, and Louise Tunnah – I could not ask for better friends and colleagues. Matt Cornish, Mike Davies, Abiran Sritharan, Sean Lee, Sydney Baxter, Andrea Dobrescu, and so many undergraduate volunteers – thanks for keeping the fish alive. Dr. Scott Taylor – your passion for rivulus and all things mangrove have been such a source of wisdom and inspiration. I have enjoyed every minute we spent together in the field, and look forward to many more. Drs. Bill Milsom and Jonathan Wilson, thank you both for your insight regarding gill structure and function, I have learned so much. I would also like to thank the extraordinary members of the Southern Ontario Killifish Society who have shared their discoveries and their fish. I received generous tissue donations from many people – thank you Hans Behr, Brittney Borowiec, Felix Breden, Peter DeSouza, Tyrone Genade, Brian Glazier, v Kate Gould, Christopher Martin, Jackie Matsumoto, Karen Murray, Jason Podrabsky, Kristina Pohl, David Reznick, Nick Sakich, and Shayla Raycroft-Tuttle. I received financial support to conduct this research from the Natural Sciences and Engineering Research Council of Canada, Ontario Graduate Scholarship program, Canadian Society of Zoologists, and the Journal of Experimental Biology Travelling Fellowship program. A special thank you to my mom and dad, and to Clare and Joe, for a lifetime of support and encouragement. Zoey – you are always there for me. I love you. vi STATEMENT OF AUTHORSHIP AND CONTRIBUTIONS TO SCIENCE All material contained in this thesis were authored by Andy Turko or as described in the author list of each chapter. Author contributions are described below: Chapter 2: AJT and PAW conceived the direction of the paper, AJT performed the literature review and wrote the draft manuscript, PAW edited the manuscript. Both authors approved the final version. Chapter 3: Conceptualization: AJT, DF, PAW; Methodology: AJT, DK, DF, RPC, FMS, MRS; Validation: AJT, DK; Formal analysis: AJT, DK; Investigation: AJT, DK, MRS; Resources: DK, RPC, FMS, PAW; Data curation: DK; Writing - original draft: AJT; Writing - review & editing: AJT, DK, DF, RPC, FMS, MRS, PAW; Visualization: AJT; Supervision: DF, RPC, FMS, PAW; Project administration: PAW; Funding acquisition: AJT, DK, RPC, PAW. Chapter 4: AJT, PAW and EMS conceived the study and designed the experiments. EMS and PM collected and analyzed micro-CT data. AJT performed the mechanical testing experiments. AJT and PM analyzed the histological data. AJT wrote the draft the manuscript; all authors revised the manuscript and provided final approval. Chapter 5: AJT conducted the experiments, analyzed the data, and wrote the draft manuscript. BC analyzed the gill photographs. PAW contributed to the overall conception of the study and design of all experiments and edited the manuscript. Chapter 6: AJT, JED, RLE, and PAW conceived the study. AJT, JED, IY-L, KL, PK, JH, and RLE carried out the experiments, AJT and JED analyzed the data. AJT wrote the draft manuscript. vii TABLE OF CONTENTS Abstract ........................................................................................................................................... ii Acknowledgements ........................................................................................................................ iv Statement of Authorship and Contributions to Science ................................................................ vii Table of Contents ......................................................................................................................... viii List of Tables ...............................................................................................................................
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