Evolutionary Dynamics of Mutualism: the Role of Exploitation and Competition

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Evolutionary Dynamics of Mutualism: the Role of Exploitation and Competition Evolutionary Dynamics of Mutualism: The Role of Exploitation and Competition Item Type text; Electronic Dissertation Authors Jones, Emily Isobel 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 26/09/2021 02:08:20 Link to Item http://hdl.handle.net/10150/193583 EVOLUTIONARY DYNAMICS OF MUTUALISM: THE ROLE OF EXPLOITATION AND COMPETITION by Emily Isobel Jones _____________________ 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 2009 2 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE As members of the Dissertation Committee, we certify that we have read the dissertation prepared by Emily Isobel Jones entitled Evolutionary Dynamics of Mutualism: The Role of Exploitation and Competition and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of Doctor of Philosophy _______________________________________________________________________ Date: 07/17/2009 Judith Bronstein _______________________________________________________________________ Date: 07/17/2009 Régis Ferrière _______________________________________________________________________ Date: 07/17/2009 Anna Dornhaus _______________________________________________________________________ Date: 07/17/2009 John Pepper 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: 07/17/2009 Dissertation Director: Judith Bronstein ________________________________________________ Date: 07/17/2009 Dissertation Director: Régis Ferrière 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 author. SIGNED: Emily Isobel Jones 4 ACKNOWLEDGEMENTS My last fortune cookie before my dissertation defense read “You are not a failure because you did not make it; you are a success because you tried.” While I managed to evade the ill omen of the cookie, it was due to the good luck of having the guidance and friendship of many people over many years. My advisors, Judie Bronstien and Régis Ferrière, balanced freedom and high expectations in a way that encouraged me to become independent and to set the same high standards for myself. I could not have hoped for better advisors to set the example of what a scientist should be and I deeply appreciate all the faith they have had in me. I am also very grateful to Anna Dornhaus, who enabled my experiments on bees and was always available to provide support and motivation, and to John Pepper, for his thoughtful insights into my work. I was very fortunate that my undergraduate advisors, Joan Strassmann and David Queller, invited me to work in their lab at Rice University. I thank Joan and Dave, as well as Chandra Jack, Natasha Mehdiabadi, Kevin Foster and Tom Platt for making the experience intellectually stimulating, satisfying and fun, thus confirming that graduate school was the right choice for me. During graduate school, I took many opportunities to explore the world beyond Tucson. I’m thankful to those who were generous with their guidance during those times: Erika Deinert and Chris Ivey (OTS, Costa Rica), Richard Law (University of York), and Bill Morris (Duke University), as well as to my co-advisor, Régis Ferrière, who made it possible for me to spend several months visiting the École Normale Supérieure and the Université Pierre et Marie Curie in Paris. I also thank the friends who made sure I wasn’t lonely, even so far from home: Hannah Lewis, Dom Carval, Violaine Cotté, and Sandra Gillespie. When back in Tucson, I benefited greatly from both the scientific discussions and distractions provided by the EEB graduate students, postdocs and visitors, particularly in the Bronstein and Dornhaus labs. I thank Nick Waser and Mary Price, who provided invaluable feedback on my research ideas and writing, and Joel and Betsy Wertheim, Tammy Haselkorn, Jenny Jandt, Latifa Jackson, Michele Lanan, and Maggie Couvillon, among many others, who provided invaluable friendship. In addition, I am especially grateful to Ali Ongun for his constant encouragement that never failed to lift my spirits. Many thanks have to go to Josefa Bleu, Julia Olszewski, Patty Stamper, and Mike Willey, who assisted in my experiments on honey bees and bumble bees, and to Maren Friesen, Tammy Haselkorn, Wendy Isner, Jenny Jandt and Michele Lanan, who volunteered their time to participate in field collections and bee research. I applaud their courage in the face of stinging bees and stabbing yuccas. My work was also greatly enhanced by funding from the Department of Ecology and Evolutionary Biology and the National Science Foundation. 5 DEDICATION To my parents, Keith and Renata Jones, for their enthusiastic encouragement of my “scientist-ing” from a very early age. 6 TABLE OF CONTENTS LIST OF FIGURES……………………………………………………………………….7 ABSTRACT……………………………………………………………………………….8 INTRODUCTION…………………………………………………………………...…..10 PRESENT STUDY……………………………………………………………………....16 REFERENCES…………………………………………………………………………..19 APPENDIX A. ECO-EVOLUTIONARY DYNAMICS OF MUTUALISTS AND EXPLOITERS……………………………………………………………………23 APPENDIX B. COEVOLUTION AND THE TRANSIENCE OF SPECIES IN AN EXPLOITED MUTUALISM……………………………………………………82 APPENDIX C. OPTIMAL FORAGING WHEN PREDATION RISK INCREASES WITH PATCH RESOURCES: AN ANALYSIS OF POLLINATORS AND AMBUSH PREDATORS………………………………………………………119 APPENDIX D. PREDATION RISK MAKES BEES REJECT REWARDING FLOWERS AND REDUCE FORAGING ACTIVITY………………………...141 7 LIST OF FIGURES FIGURE 1………………………………………………………………………..………11 FIGURE 2………………………………………………………………………..………13 8 ABSTRACT Species exist in complex biotic environments, engaging in a variety of antagonistic and cooperative interactions. While these interactions are generally recognized to be context-dependent, varying in outcome in the presence of other interactions, studies tend to focus on each interaction in isolation. One of the main classes of species interaction is mutualism, in which partner species gain a net benefit from their interaction. However, mutualisms are beset by a variety of species that can reduce or even eliminate the benefits of mutualism through exploitation of and competition for the resources and services offered by mutualists. These exploiter species potentially threaten the ecological stability of mutualisms and may alter selection on mutualistic traits. Thus, understanding the ecology and evolution of mutualisms requires consideration of interactions with exploiter species. In this dissertation, I investigated the effects of exploiter species on mutualisms between plants and pollinators using a combination of eco-evolutionary modeling, optimization theory, and behavioral studies. Using two adaptive dynamics models of coevolution in exploited pollinating seed parasite mutualisms, I found that exploiters reduce mutualist densities and select for more parasitic mutualists. Nevertheless, the models demonstrate that intraspecific competition for host resources and host defense of those resources restrict the ecological conditions that lead to extinction of the mutualism, as well as the chances of evolution to extinction. Thus, exploiters are unlikely to be the threat to mutualisms that has been assumed previously. On the other hand, in another type of exploitation, exploitative predators may 9 pose a greater threat to investment in mutualism than has been presumed. Through both optimal foraging theory and behavioral experiments on bumble bees, I found that the risk from ambush predators can change pollinator floral preferences when predators preferentially use high-quality flowers to locate their prey. This research suggests that predators of mutualists may have important top-down effects and that further research is needed to investigate the effects of exploitative predators on selection on mutualist traits. 10 INTRODUCTION Explanation of the problem and a review of the literature Mutualisms are defined by the net benefit partner species derive from the interaction. Mutualisms play a key role in ecosystem function and the delivery of major ecological services, including nitrogen fixation, pollination, and protection against herbivores, predators and parasites (Agrawal et al. 2007; Holland and Bronstein 2008). Mutualists generally must invest resources into the interaction (Bronstein 2001a); consequently, individuals of mutualist species that cheat their partners by investing little or nothing are expected to have an advantage over their more cooperative
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