The Ecology Of Co-Infection In The Phyllosphere: Unraveling The Interactions Between Microbes, Insect Herbivores, And The Host Plants They Share Item Type text; Electronic Dissertation Authors Humphrey, Parris Taylor 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 23/09/2021 20:08:03 Link to Item http://hdl.handle.net/10150/565900 THE ECOLOGY OF CO-INFECTION IN THE PHYLLOSPHERE: UNRAVELING THE INTERACTIONS BETWEEN MICROBES, INSECT HERBIVORES, AND THE HOST PLANTS THEY SHARE by Parris T. Humphrey __________________________ A Dissertation Submitted to the Faculty of the DEPARTMENT OF ECOLOGY & EVOLUTIONARY BIOLOGY In Partial Fulfillment of the Requirements For the Degree of DOCTOR OF PHILOSOPHY In the Graduate College THE UNIVERSITY OF ARIZONA 2015 2 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE As members of the Dissertation Committee, we certify that we have read the dissertation prepared by Parris T. Humphrey, titled The ecology of co-infection in the phyllosphere: Dissecting three-way interactions between plants and their microbial and insect attackers, and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy. _______________________________________________________________________ Date: (May 8, 2015) Noah K. Whiteman _______________________________________________________________________ Date: (May 8, 2015) Martha S. Hunter _______________________________________________________________________ Date: (May 8, 2015) Michael Worobey _______________________________________________________________________ Date: (May 8, 2015) David Baltrus 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: (May 8, 2015) Dissertation Director: Noah K. Whiteman 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 author. SIGNED: Parris T. Humphrey 4 ACKNOWLEDGEMENTS In late spring of 2010, Noah Whiteman extended an invitation to me to join his new lab. He may not have known it at the time, but such an invitation was the very thing that stopped me from quietly bowing out of graduate school after an initial year of turmoil and uncertainty. His openness, compassion, and generosity allowed me to carve out a meaningful set of research questions under his mentorship. I owe any successes I might have had since to this initial and decisive act of encouragement. I am also grateful to several of the outstanding faculty in EEB (past and present) from whom I have received enduring inspiration: Judith (Judie) Bronstein, Peter Chesson, Brian Enquist, Regis Ferriere, Joanna Masel, Nancy Moran, Michael Nachman, Howard Ochman, and Michael Worobey. I would also like to thank the members of my committee, Michael Worobey, Martha (Molly) Hunter, and David Baltrus, for their feedback and perpetual support throughout this process. I have been lucky to receive financial support from the NSF in the form of an IGERT training fellowship in Genomics for my first three years as a graduate student, as well as a Doctoral Dissertation Improvement Grant, which supported my later chapters and continues to support ongoing work. Various awards from within the University of Arizona have greatly improved my experience, including from the Center for Insect Science, the Galileo Circle, the Graduate and Professional Student Council, and the Department of Ecology & Evolutionary Biology. My three field seasons at the Rocky Mountain Biological Laboratory (RMBL) would not have been 5 possible without the generous support of their graduate fellowships or their NSF-funded REU program that supported most of the undergraduates I was lucky to mentor: thank you to Jennie Reithel, Ian Billick, and Emily Mooney for making this possible. My final year was greatly enhanced by the opportunity to study for two months at the École Normal Supérieure (ENS) in Paris, France, thanks to Regis Ferriere and the PUF/FACE grant to the University of Arizona and ENS. The intellectual growth afforded by this experience already has made a substantial impact on my future research trajectory. Thank you also to all of the members of the Whiteman lab since its inception: you have created a warm and stimulating environment in which to work and have set the bar of collegiality and camaraderie very high. My family has also played a central role in supporting my endeavors in part by not begrudging me my infrequent phone calls or incessant business: thank you to Ralph, JoAnn, Callie, and Pharel, for this loving kindness. Finally, I am especially grateful to Jeremy Jonas, Melissa Duhaime, Kevin Vogel, Paul CaraDonna, Ross Brennan, and Timothy O’Connor for their wonderful gifts of friendship, and to Heather Briggs for the incredible gift of partnership. 6 DEDICATION To KMB for helping me into this, and to HMB for helping me out. 7 TABLE OF CONTENTS ABSTRACT.....................................................................................................................................8 INTRODUCTION.........................................................................................................................10 1.1 Dissertation overview..................................................................................................10 1.2 Origins and implications of immune cross-talk...........................................................14 1.3 General implications....................................................................................................19 1.4 Future directions..........................................................................................................20 1.5 Explanation of dissertation format..............................................................................21 PRESENT STUDY........................................................................................................................22 2.1 Diversity and abundance of phyllosphere bacteria are linked to insect herbivory.....22 2.2 Plant secondary compounds are attractive, aversive, and defensive in the foraging ecology of a specialist herbivore.......................................................................................23 2.3 Life history variation underlies competition and co-existence in a phyllosphere Pseudomonas spp. community...........................................................................................24 REFERENCES..............................................................................................................................26 APPENDIX A: DIVERSITY AND ABUNDANCE OF PHYLLOSPHERE BACTERIA ARE LINKED TO INSECT HERBIVORY...........................................................................................32 APPENDIX B: PLANT SECONDARY COMPOUNDS ARE ATTRACTIVE, AVERSIVE, AND DEFENSIVE IN THE FORAGING ECOLOGY OF A SPECIALIST HERBIVORE.......83 APPENDIX C: LIFE HISTORY VARIATION UNDERLIES COMPETITION AND CO- EXISTENCE IN A PHYLLOSPHERE PSEUDOMONAS SPP. COMMUNITY......................132 8 ABSTRACT Infection by multiple parasites is a part of everyday life for many organisms. The host immune system may be a central mediator of the many ways parasites might influence one another (and their hosts). Immunity provides a means for the colonized to reduce the success of current and future colonizers and has evolved across the tree of life several times independently. Along the way, the immune systems of plants as well as many groups of animals has evolved perhaps an accidental vulnerability wherein defense against one parasite can increase susceptibility to others. This so-called immune ‘cross-talk’ is a conundrum worth investigating not only to understand the impact of parasites on focal organisms, but also to better predict how immunity itself influences the evolution and epidemiology of parasites whose spread we might like to curtail. For plants, co-infection often comes in the form of insect herbivores and various bacteria that colonize the leaf interior. Both colonizers can reduce plant fitness directly or indirectly by potentiating future enemies via cross-talk in plant immunity. This phenomenon has largely been studied in laboratory model plants, leaving a substantial gap in our knowledge from native species that interact in the wild. This dissertation helps close this gap by investigating the ecology of co-infection of a native plant by its major insect herbivore and diverse leaf-colonizing bacteria. I revealed that leaf co-infection in the field by leaf-mining herbivores and leaf- colonizing ("phyllosphere") bacteria