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Gonium Pectorale Genome Demonstrates Co-Option of Cell Cycle Regulation During the Evolution of Multicellularity

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Gonium Pectorale Genome Demonstrates Co-Option of Cell Cycle Regulation During the Evolution of Multicellularity The Evolution of Cell Cycle Regulation, Cellular Differentiation, and Sexual Traits during the Evolution of Multicellularity Item Type text; Electronic Dissertation Authors Hanschen, Erik Richard 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 07/10/2021 00:03:04 Link to Item http://hdl.handle.net/10150/626165 THE EVOLUTION OF CELL CYCLE REGULATION, CELLULAR DIFFERENTIATION, AND SEXUAL TRAITS DURING THE EVOLUTION OF MULTICELLULARITY by Erik Richard Hanschen __________________________________ Copyright © Erik Richard Hanschen 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 Erik R. Hanschen, titled “The evolution of cell cycle regulation, cellular differentiation, and sexual traits during the evolution of multicellularity” and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy. _______________________________________________________________________ Date: September 25, 2017 Richard E. Michod _______________________________________________________________________ Date: September 25, 2017 Régis Ferrière _______________________________________________________________________ Date: September 25, 2017 Michael Barker _______________________________________________________________________ Date: September 25, 2017 Bradley J. S. C. Olson 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: September 25, 2017 Dissertation Director: Richard E. Michod 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: Erik Richard Hanschen 4 ACKNOWLEDGEMENTS I would like to first thank my doctoral committee for their invaluable contributions to my research over the course of my time at the University of Arizona. Working for Rick Michod has taught me how to be an independent and creative scientist and how to take research projects from an initial idea through development and analysis to publication. Brad Olson has been a close and valuable collaborator who has contributed much to my development as a scientist as we analyzed volvocine genomes. Mike Barker has been an invaluable resource for genomic approaches, concepts, and ideas. More importantly, Mike Barker is a steadfast source of encouragement and cheerleading throughout the progress of research. Régis Ferrière has been invaluable to the direction of my dissertation research, expertly and brilliantly suggesting sweeping changes in research direction with a single question. I greatly appreciate the community of scientists that have lead to this body of work, the Volvox community has been a wealth of ideas and suggestions as my research progresses. I would especially like to thank Aurora Nedelcu and Matthew Herron who have both been dear friends and sources of advice. I would like many others, including Dinah R. Davison, Deborah S. Shelton, Zach I. Grochau-Wright, Patrick J. Ferris, Tara N. Marriage, Hisayoshi Nozaki, John J. Wiens, Baltazar Chavez-Diaz Jr., David Shahnooshi, and Jeremiah Hackett. Of course an entire community at UA EEB is due acknowledgement, including Sky Dominguez, LuAnn Casem, Lauren Harrison, Pennie Rabago, Barbara Johnson, Vincente Leon, Barry McCabe, Lilian Schwartz, Pat Waters, and Carol Freeman. Other valuable colleagues, among others, include Jen Wisecaver, William Driscoll, and Doug Cromey. Throughout my PhD, a large number of friends and family have been critical to staying the course, whether through beer, advice, or getting outside together. This includes Tom Hanschen, Linnea Hanschen, Brendan Hanschen, Ryan Hanschen, Shannon Hanschen, Holden Hanschen, Hugo Hanschen, Sky Dominguez, Moira Hough, Tyeen Taylor, Marielle Smith, Brad Boyle, Rebekah Doyle, Alex Brummer, Jason Veatch, Justin Schaffer, Jonathan Mosher, Ryan Dunn, Katie Fisher, Connie Lam, Amanda Goldstein, Blake Heym, Pacifica Sommers, Neill Prohaska, and Ariana La Porte. Sources of funding for this research include the NSF IGERT training grant “Program in Comparative Genomics”, the NIH training grant “Computational and Mathematical Modeling of Biological Sciences”, the National Institute of Genetics (Japan), and the UA Department of Ecology and Evolutionary Biology. I also received support from a NSF grant awarded to Brad Olson and Rick Michod and a NASA grant awarded to Rick Michod and Patrick Ferris. Other valuable sources of funding in the American Genetics Association, Graduate and Professional Student Council travel and Research and Project grants, the UA Galileo Circle Scholarship program, and Robert W. Hoshaw Memorial Scholarship, the Kavli Institute for Theoretical Physics, and the National Evolutionary Synthesis Center. 5 TABLE OF CONTENTS ABSTRACT.................................................................................................................................... 6 INTRODUCTION.......................................................................................................................... 8 PRESENT STUDY....................................................................................................................... 15 REFERENCES............................................................................................................................. 24 APPENDIX A. EVOLUTIONARY TRANSITIONS IN INDIVIDUALITY AND RECENT MODELS OF MULTICELLULARITY....................................................................................... 32 APPENDIX B. THE GONIUM PECTORALE GENOME DEMONSTRATES CO-OPTION OF CELL CYCLE REGULATION DURING THE EVOLUTION OF MULTICELLULARITY... 57 APPENDIX C. EARLY EVOLUTION OF THE GENETIC BASIS FOR SOMA IN THE VOLVOCACEAE......................................................................................................................... 68 APPENDIX D. MULTICELLULARITY DRIVES THE EVOLUTION OF SEXUAL TRAITS......................................................................................................................................... 81 6 ABSTRACT During the evolution of multicellularity from unicellular ancestors, cells transition from being evolutionary individuals to components of more complex, multicellular evolutionary individuals. The volvocine green algae provide a powerful model system for understanding the genetic and morphological changes that underlie and are caused by the evolution of multicellularity. This dissertation concerns the role of cell cycle regulation, cellular differentiation, and sexual traits during the evolution of multicellularity. While some of these are shown to be causally important in the origins of multicellularity (Appendix B), others are driven by the evolution of multicellularity (Appendix D). We provide a review of recent mathematical models on the evolution of multicellularity, which are found to focus heavily on the later, subsequent stages of the evolution of multicellular complexity. We found that many of these models assume multicellular ancestors and instead evolve cellular differentiation, bringing attention to a gap in our understanding of the events in the initial stages of the evolution of multicellularity. We show that a focus on the early stages of the evolution of multicellularity reveals a powerful and critical role for regulation of the cell cycle at the origins of multicellularity (Appendix B). We further find that the genetic basis for cellular differentiation evolved sometime after the evolution of cell cycle regulation. We find that while the genetic basis for cellular differentiation evolved after cell cycle regulation, it also evolved earlier than previously predicted in the volvocine green algae, suggesting an important role in undifferentiated species (Appendix C). Lastly, having elucidated the origins and evolution of multicellularity, we find that multicellularity causes the evolution of sexual traits including anisogamy, internal fertilization, and subsequently sexual dimorphism (Appendix D). This work emphasizes the important role that multicellularity plays
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