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Developmental Evolution of the Progamic Phase in Nymphaeales

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University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 5-2011 Developmental Evolution of the Progamic Phase in Nymphaeales Mackenzie Lorraine Taylor University of Tennessee - Knoxville, [email protected] Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Part of the Evolution Commons, and the Plant Biology Commons Recommended Citation Taylor, Mackenzie Lorraine, "Developmental Evolution of the Progamic Phase in Nymphaeales. " PhD diss., University of Tennessee, 2011. https://trace.tennessee.edu/utk_graddiss/1031 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Mackenzie Lorraine Taylor entitled "Developmental Evolution of the Progamic Phase in Nymphaeales." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Doctor of Philosophy, with a major in Ecology and Evolutionary Biology. Joseph H. Williams, Major Professor We have read this dissertation and recommend its acceptance: Edward E. Schilling, Randall L. Small, Andreas Nebenfuhr Accepted for the Council: Carolyn R. Hodges Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) DEVELOPMENTAL EVOLUTION OF THE PROGAMIC PHASE IN NYMPHAEALES A Dissertation Presented for the Doctor of Philosophy Degree The University of Tennessee, Knoxville Mackenzie Lorraine Taylor May 2011 DEDICATION To my grandma: Vera Lorraine Stevens Holmes (1921 – 2011) Who inspires me to be a strong, independent, creative woman and who, above all, loved me. And to my grandma: Hazel Aileen Hagadorn Taylor (1906-1994) Who let me water her cacti and climb her trees and whose (very thorny) rose bushes I encountered in one of my very first interactions with the botanical world. ii ACKNOWLEDGEMENTS I wish to thank my advisor, Joe Williams, for allowing me the freedom to pursue my own interests and giving me the guidance to reach my goals. I also wish to express my gratitude to the members of my committee, Ed Schilling, Andreas Nebenführ, Randy Small, and Taylor Feild for their assistance, motivation, and positive feedback. I thank the Department of Ecology and Evolutionary Biology for steadfast intellectual and financial support during my tenure at the University of Tennessee and I extend great thanks to Ken McFarland for maintaining greenhouse water tanks and for numerous illuminating conversations. I would like to thank several of my colleagues for their friendship, encouragement, and intellectual stimulation: Audra Galasso, Patrick Hudson, Steve Furches, Dwayne Estes, John Beck, Susan Farmer, Ed Lickey, Annie Becker, Lawong Balun, Michelle Smith, and Lisa Cantwell. I especially thank the past and present members of the Williams’ Lab, Matt Valente, Tatiana Arias, Nicholas Buckley, Matt Heard, and Jason Abercrombie, for making the last few years a lot of fun and for being there to lend a hand (or a shoulder to cry on). I also owe special thanks to Jeffrey M. Osborn at The College of New Jersey for his continued collaboration and commitment to my professional growth. I thank all those who have helped me in the field or lab: James Parker, Ralph McNeilage, Matt Lettre, Andrew Moffat, Kathryn Smith, Cyndi Rossini, and Andrew Herget. I was very fortunate to have excellent help while carrying out my work. I would like to express my deep gratitude to Robyn Bowles, Rich Robinson, Roger Hearn, and especially to Terry McFarlane at the Western Australia Department of Environment and Conservation office in Manjimup, whose logistical support made my work with Trithuria possible, and whose incredible hospitality made it tremendously enjoyable. They opened up their labs, homes, and community to me and I will always be thankful for that experience. I also thank the Government of Australia Department of Environment and Conservation for issuing the required collection permits (SL008272, SL008694, CE002100, CE002511) and the Department of Environment, Water, Heritage, and the Arts for issuing the export permits (WT2008-3749, WT2009-4196) necessary to complete this work. I would like to acknowledge David Brewster at the Tennessee Valley Authority for help me locate Cabomba populations and Ed Schneider at the University of Minnesota for information about tropical water lilies, as well as several photographs. The following sources provided funding for my dissertation work: The National Science Foundation (Graduate Research Fellowship [2006-2009] and Dissertation Improvement Grant [DEB 0910171]), The Botanical Society of America Graduate Student Research Award (2008), and the University of Tennessee (Department of Ecology and Evolutionary Biology Summer Research Award [2006, 2008, 2009, 2010]; the Hesler Fund; and the AJ Sharp Fund [2006]). Finally, I would like to thank my parents, Jim and Janice Taylor, as well as the rest of my family for their love, support, and understanding. iii ABSTRACT The period between pollination and fertilization, or the progamic phase, is a critical life history stage in seed plants and innovations in this life history stage are hypothesized to have played an important role in the diversification of flowering plants. Over the course of this dissertation research, I investigated programic phase development in Nymphaeales (water lilies), an ancient angiosperm lineage that diverged from the basalmost or next most basal node of the angiosperm phylogenetic tree and that is represented in the oldest angiosperm fossil record. I used field experiments and microscopy to document pollination biology, breeding system, and reproductive developmental traits in two families of Nymphaeales: Cabombaceae (Brasenia, Cabomba) and Hydatellaceae (Trithuria). Nymphaeales exhibits considerable variation in reproductive traits and true carpel closure, wind-pollination, and a primarily selfing breeding system have arisen independently in the lineage. Pollen tube pathway length, timing of stigma receptivity, and pollen tube growth rates are conspicuous traits that have undergone considerable modification in concert with shifts in pollination biology and breeding system. Post-pollination developmental processes in Nymphaeales appear to experience selective pressures similar to those experienced by more derived angiosperms and to evolve in similar ways. Nymphaeales also exhibits traits, such as accelerated pollen tube growth, callosic pollen tube walls, and the formation of callose plugs, that are almost certainly plesiomorphic in angiosperms and may have facilitated modification of carpel structure and progamic phase ontogenies. The finding that pollen tube traits that underlie developmental flexibility were already in place before the divergence of Nymphaeales supports the hypothesis that innovations in male gametophyte development were instrumental in facilitating early angiosperm diversification. iv TABLE OF CONTENTS CHAPTER PAGE Chapter I: Introduction to the progamic phase and Nymphaeales........................................1 Introduction ............................................................................................................................2 The Progamic Phase................................................................................................................2 Early-Divergent Angiosperm Lineages....................................................................................4 Nymphaeales as a Study System .............................................................................................5 Goals of the Dissertation Research..........................................................................................8 Literature Cited.....................................................................................................................10 Appendix 1 ...........................................................................................................................14 Chapter II: Consequences of pollination syndrome evolution for post-pollination biology in an ancient angiosperm family.................................................................................................17 Abstract ................................................................................................................................18 Introduction ..........................................................................................................................18 Methods................................................................................................................................21 Results ..................................................................................................................................26 Discussion.............................................................................................................................33 Conclusion............................................................................................................................44 Literature Cited.....................................................................................................................45 Appendix
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