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An Example with Carotenoid Diversification in Birds Exploring the Deterministic Landscape of Evolution: An Example with Carotenoid Diversification in Birds Item Type text; Electronic Dissertation Authors Morrison, Erin Seidler Publisher The University of Arizona. Rights Copyright © is held by the author. Digital access to this material is made possible by the University Libraries, University of Arizona. Further transmission, reproduction or presentation (such as public display or performance) of protected items is prohibited except with permission of the author. Download date 02/10/2021 06:24:33 Link to Item http://hdl.handle.net/10150/624290 EXPLORING THE DETERMINISTIC LANDSCAPE OF EVOLUTION: AN EXAMPLE WITH CAROTENOID DIVERSIFICATION IN BIRDS by Erin Seidler Morrison __________________________ Copyright © Erin Seidler Morrison 2017 A Dissertation Submitted to the Faculty of the DEPARTMENT OF ECOLOGY AND EVOLUTIONARY BIOLOGY In Partial Fulfillment of the Requirements For the Degree of DOCTOR OF PHILOSOPHY In the Graduate College THE UNIVERSITY OF ARIZONA 2017 2 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE As members of the Dissertation Committee, we certify that we have read the dissertation prepared by Erin Morrison, entitled EXPLORING THE DETERMINISTIC LANDSCAPE OF EVOLUTION: AN EXAMPLE WITH CAROTENOID DIVERSIFICATION IN BIRDS and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy. _______________________________________________________________________ Date: February 21, 2017 Alexander Badyaev _______________________________________________________________________ Date: February 21, 2017 Renée Duckworth _______________________________________________________________________ Date: February 21, 2017 Michael Sanderson _______________________________________________________________________ Date: February 21, 2017 Sergey Gavrilets Final approval and acceptance of this dissertation is contingent upon the candidate’s submission of the final copies of the dissertation to the Graduate College. I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement. ________________________________________________ Date: February 21, 2017 Dissertation Director: Alexander Badyaev 3 STATEMENT BY AUTHOR This dissertation has been submitted in partial fulfillment of the requirements for an advanced degree at the University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library. Brief quotations from this dissertation are allowable without special permission, provided that an accurate acknowledgement of the source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgment the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author. SIGNED: Erin Seidler Morrison 4 ACKNOWLEDGEMENTS I would first like to thank Alex Badyaev, without whom this dissertation would not have been possible. It is thanks to Alex that I have learned how to independently think and question the world around me. While I know it has been challenging, I sincerely appreciate that he did not give up on me at a time when I almost gave up on myself. With his support I took on a project that perhaps was more ambitious than I bargained for, but Alex patiently helped through needlessly complicated measures and half-baked hypotheses, and did not charge me too much for repeated grammatical errors. Alex has taught me how to be a scientist and a teacher, and how to both appreciate and criticize the science we do. I will always be grateful that he took a chance on me and for his continued mentorship and support. There are a number of people who have provided much needed support, discussion, and opinions on the work presented here, and throughout my graduate school career. I appreciate the expertise, unique perspectives, and encouragement provided by the members of my committee: Renée Duckworth, Michael Sanderson, and Sergey Gavrilets. Their insightful questions and advice along the way gave me opportunities to think about my work from different perspectives, and I have learned so much from having the opportunity to interact with them. I cannot express how appreciative I am for all of the help I have received from past and current members of my lab group: Stepfanie Aguillon, Samantha Anderson, Virginia Belloni, Katie Chenard, Christopher Gurguis, Kelly Hallinger, Dawn Higginson, Ellen Ouellette, Jared Padway, Ahvi Potticary, and Georgy Semenov. They have sat through countless lab meetings on my work and their suggestions, advice, creativity, humor and patience were always welcome. I particularly want to thank Dawn Higginson, she continues to listen to me and give advice no matter how busy she is, and I have learned a tremendous amount from her. Almost all of the data collected for these studies would not have been possible without the help of a small army of people. I would like to thank Emmet Andrews, Virginia Belloni, Matt Coope, Courtney Christie, Caitlin Davey, Sarah Davis, Rachael Delaney, Victoria Farrar, Lauren Harris, Kelly King, Xander Posner, Jordan Veal, and Adam Welu for their tireless work. It has been so exciting to watch those who came in as undergraduates develop as scientists in their own right, and their enthusiasm for research was always the best part of my day. I would also like to thank Renée Duckworth for patiently helping me with HPLC. I appreciate the support of the EEB administrative staff for their help throughout the years. Funding for the research presented here was provided in part by grants from the National Science Foundation and the Packard Foundation to Alex Badyaev. I was also supported by fellowships from Amherst College and the University of Arizona Galileo Circle. I want to thank those who adopted me into their families and made sure that I always had someone to eat, swim, run, ride, and watch movies and TV with, and it is entirely thanks to all of them that the desert has become home: Sam Anderson, Sarah Baillie, Erin Dombrady, Cole Eskridge, Tim Gendler, Judy Helfand, Dennis Helfand, Dawn Higginson, Bridget Keene, Charlie Keene, Evan Keleman, Gavin Leighton, Janet Levine, Josh Levine, Kristen Metzger, Ellen Ouellette, and Ahvi Potticary. I cannot express the gratitude I owe to my family, Wendy, Rob and Kasey Morrison. While they still may not understand what it is that I do, they have been supportive in every decision I have made and they always let Ted get in his two cents. I also appreciate Stephen Selzer for his support. Lastly, I want to thank my grandmother, Violet Selzer, who told me every Monday night for the first five and a half years of graduate school that she was sure I would do great and that her opinion was definitely impartial. 5 TABLE OF CONTENTS ABSTRACT……………………………………………………………………………………….6 I. INTRODUCTION………………………………………………………………………………8 II. PRESENT STUDY…………………………………………………………………………...13 REFERENCES…………………………………………………………………………………..18 APPENDIX A. STRUCTURING EVOLUTION: BIOCHEMICAL NETWORKS AND METABOLIC DIVERSIFICATION IN BIRDS………………………………………...21 APPENDIX B. THE LANDSCAPE OF EVOLUTION: RECONCILING STRUCTURAL AND DYNAMIC PROPERTIES OF METABOLIC NETWORKS IN ADAPTIVE DIVERSIFICATIONS…………………………………………………………………...56 APPENDIX C. BEYOND NETWORK TOPOLOGY: COEVOLUTION OF STRUCTURE AND FLUX IN METABOLIC NETWORKS…………………………………………...70 APPENDIX D. RETENTION AND RECOMBINATION OF BIOCHEMICAL MODULES IN THE EVOLUTION OF AVIAN CAROTENOID METABOLISM………………..108 6 ABSTRACT Establishing metrics of diversification can calibrate the observed scope of diversity within a lineage and the potential for further phenotypic diversification. There are two potential ways to calibrate differences between phenotypes. The first metric is based on the structure of the network of direct and indirect connections between elements, such as the genes, proteins, enzymes and metabolites that underlie a phenotype. The second metric characterizes the dynamic properties that determine the strength of the interactions among elements, and influence which elements are the most likely to interact. Determining how the connectivity and strength of interactions between elements lead to specific phenotypic variations provides insight into the tempo and mode of observed evolutionary changes. In this dissertation, I proposed and tested hypotheses for how the structure and metabolic flux of a biochemical network delineate patterns of phenotypic variation. I first examined the role of structural properties in shaping observed patterns of carotenoid diversification in avian plumage. I found that the diversification of species-specific carotenoid networks was predictable from the connectivity of the underlying metabolic network. The compounds with the most enzymatic reactions, that were part of the greatest number of distinct pathways, were more conserved across species’ networks than compounds associated with the fewest enzymatic reactions. These results established that compounds with the greatest connectivity act as hotspots for the diversification of pathways between species. Next, I investigated how dynamic properties of biochemical networks influence patterns of phenotypic variation in the concentration and occurrence of compounds. Specifically, I examined if the rate of compound
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