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6 VARIATION in the OBLIGATE SYMBIONTS of APHIDS by Kevin Variation in the Obligate Symbionts of Aphids Item Type text; Electronic Dissertation Authors Vogel, Kevin 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 24/09/2021 13:19:10 Link to Item http://hdl.handle.net/10150/222898 6 VARIATION IN THE OBLIGATE SYMBIONTS OF APHIDS by Kevin J. Vogel ________________________ 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 2012 2 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE As members of the Dissertation Committee, we certify that we have read the dissertation prepared by Kevin J. Vogel entitled VARIATION IN THE OBLIGATE SYMBIONTS OF APHIDS and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy _______________________________________________________________________ Date: 3-9-2012 Nancy A. Moran _______________________________________________________________________ Date: 3-9-2012 Michael W. Nachman _______________________________________________________________________ Date: 3-9-2012 Jeremiah D. Hackett _______________________________________________________________________ Date: 3-9-2012 Noah K. Whiteman 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: 3-9-2012 Dissertation Director: Nancy A. Moran 3 STATEMENT BY AUTHOR This dissertation has been submitted in partial fulfillment of 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 accurate acknowledgment of 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: Kevin J. Vogel 4 ACKNOWLEDGEMENTS Nancy Moran has been a wonderfully supportive, helpful, responsive, and above all, patient, advisor. Her guidance in designing experiments, analyzing data, writing manuscripts and preparing presentations was invaluable. It has truly been an honor to work under such an amazing scientist. Michael Nachman, Jeremiah Hackett and Noah Whiteman have donated their time, lab space and resources in my pursuit of my degree. Their advice and feedback were instrumental in my success. I would like to thank Jeremiah for tolerating all my drop-in visits and “borrowing” of reagents, Noah for including me in his lab group, and Michael for his mentorship and wonderful teaching. Thank you also to Howard Ochman and Carlos Machado for their roles in my earlier committees, and to Howard for his advice in lab meetings and teaching me how to write. The members of the Moran-Ochman lab have been an endless source of advice, feedback, guidance, friendship and support: Gaelen Burke, Patrick Degnan, Nicole Gerardo, Allison Hansen, Chi-Horng Kuo, Renyi Liu, Pradeep Reddi Marri, Vince Martinson, John McCutcheon, Hema Narra, Kerry Oliver, Rahul Raghavan, Zakee Sabree, John Stravinides, Mark van Passel, and Alex Wilson. Thank you Helen Dunbar, Kim Hammond, Phat Tran, Heather McLaughlin, and Tyler Jarvik for all your technical and practical assistance. Thank you to Emily Hartley, Kevin Z. Sunitsch, and Kevin MacDow for their help as undergraduate assistants. Thank you to Cathy Wasmann, without whose advice and guidance, chapter 3 would have been impossible. Thanks to Matt Sullivan and Hans Van Etten for their space, equipment, and reagents. Thank you to Becky Nankivell, Teresa Kudrna, Sharon Richards, Pam Murray, Lili Schwartz, Liz Oxford, and the EEB office staff for making reagents, supplies, and paychecks appear. I would also like to acknowledge the department of Ecology and Evolutionary Biology, the Center for Insect Science, and the National Science Foundation’s IGERT and G-K12 (BioME) programs for funding my research and training. Grants from the National Science Foundation to Nancy Moran paid for much of my research. Lukasz Stelinski and Jim Miller deserve credit for setting me on this path. Special thanks is due to Joel and Betsy Werthiem, Alex Eilts, and John Stravinides, and John McCutcheon, who have kept me on that path through all the tough times. Mark van Passel, your support, advice, and friendship is beyond measure. Vince Martinson and Ellen Suurmeyer, thanks for always being such great friends, no matter what, and for being up for any adventure. Melissa Duhaime and Vincent Denef, for all their help, advice, and friendship. Kristen Potter and Thom Lord, thank you for listening. Thank you to Margaret Wilch for being such an inspiration, great mentor, and wonderful friend. Thanks to all my other friends for the help and support they’ve provided over the years. Thank you to my family, whose support, love, and encouragement has been unwavering since day one. Thank you to my wife, Gaelen, for pointing out the holes in my arguments, helping me with programming, reading my manuscripts, and keeping me caffeinated and on track, and for believing in me. 5 DEDICATION To my wife, Gaelen 6 TABLE OF CONTENTS ABSTRACT………………………………………………………………………………7 INTRODUCTION………………………………………………………………………...9 PRESENT STUDY………………………………………………………………………21 REFERENCES…………………………………………………………………………..25 APPENDIX A: SOURCES OF VARITATION IN DIETARY REQUIREMENTS IN AN OBLIGATE NUTRITIONAL SYMBIOSIS………………………………………..30 APPENDIX B: EFFECT OF HOST GENOTYPE ON SYMBIONT TITER IN THE APHID-BUCHNERA SYMBIOSIS……………………………………………………...72 APPENDIX C: GENOMIC EVOLUTIONARY AND FUNCTIONAL ANALYSIS OF THE YEAST-LIKE SYMBIONT OF THE APHID CERATAPHIS BRASILIENSIS…..101 7 ABSTRACT Intimate, mutualistic, association with microbes is a common mechanism for organisms to utilize certain niches. Insects are a particularly well-studied group in this respect, frequently forming long-term, obligate associations with symbiotic microbes. These symbioses are often nutritional in nature, with the symbiont providing the host with nutrients that are otherwise unavailable. Aphids are notable for their well-defined relationship with the symbiotic Bacteria Buchnera aphidicola. By synthesizing the amino acids the aphid is unable to produce itself, Buchnera permits its host to feed on plant phloem, which lacks sufficient quantities of these essential nutrients. Buchnera, as with many obligate intracellular symbionts, has a reduced effective population size (Ne) due to asexual reproduction and severe population bottlenecks experienced during transmission between generations. The reduction in Ne has facilitated the degradation of the symbiont genome through fixation of deleterious mutations via drift. The consequences of accelerated evolutionary rates has been examined primarily through genome sequencing and comparative studies of symbionts from different host species. The work detailed in this dissertation examines the role of deleterious mutations and drift at multiple taxonomic levels. Analysis of aphid amino acid requirements utilizing an artificial diet assay revealed variation in clones of the pea aphid, Acyrthosiphon pisum. In one clone, a mutation in the arginine biosynthesis pathway appears to underlie a host dietary requirement for arginine. Examination of the number of Buchnera within an A. pisum clone also revealed variation in symbiont titer between clones. When compared across F1 offspring of cross between a low- and a high-titer clone, extensive variation was observed 8 in titer that exceeded variation observed in field-collected clones. No maternal effects were observed, suggesting that Buchnera is not in control of its replication. At a broader taxonomic scale, the replacement of Buchnera in the aphid Cerataphis brasiliensis was examined by sequencing the genome of its fungal symbiont (YLS). The genome of the YLS revealed a much greater metabolic capacity than Buchnera, possibly due to its extracellular habitat. The YLS exhibited signatures of elevated evolutionary rates and intron gain consistent with a reduction in Ne due to its symbiotic niche. 9 INTRODUCTION Explanation of the problem and its context Over the course of evolution, plants and animals have come to rely on a variety of microorganisms to provide an array of functions ranging from defense from predators to supplying nutrients to disabling prey defenses. These relationships span a continuum from facultative to obligate and from mutualistic to exploitative. Of beneficial microbe- animal relationships, much attention has been paid to microbes providing nutritional benefits to their host. Nutrient-provisioning by microbes to a host has allowed organisms to exploit otherwise
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