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UNIVERSITY of CALIFORNIA SANTA CRUZ Epidemiology, Resistance UNIVERSITY OF CALIFORNIA SANTA CRUZ Epidemiology, Resistance Structure, and the Effects of Soil Calcium on a Serpentine Plant-Pathogen Interaction A thesis submitted in partial satisfaction of the requirements for the degree of DOCTOR OF PHILOSOPHY in ECOLOGY AND EVOLUTIONARY BIOLOGY by Yuri P. Springer March 2006 The dissertation of Yuri P. Springer is approved: ___________________________________ Professor Mark H. Carr, Co-Chair ___________________________________ Professor Gregory S. Gilbert, Co-Chair ___________________________________ Professor Ingrid M. Parker ____________________________________ Lisa C. Sloan Vice Provost and Dean of Graduate Studies Copyright © by Yuri P. Springer 2006 Table of Contents 1. Title Page i 2. Copyright Notice ii 3. Table of Contents iii 4. Abstract iv 5. Acknowledgements vi 6. Introduction 1 7. Chapter 1: Effects of Soil Calcium Concentrations on Infection 8 Rates in a Serpentine Plant/Pathogen Interaction: A Test of the Pathogen Refuge Hypothesis 8. Chapter 2: Epidemiological Patterns and Fitness Impacts 37 Associated with Fungal Infection of a Serpentine Flax 9. Chapter 3: Characterizing Host Resistance Structure and 75 Pathogen Local Adaptation in a Serpentine Flax/Flax Rust Interaction 10. Appendix 1: Phylogenetic Analysis of the Genus Hesperolinon 108 11. Appendix 2: Edaphic and Epidemiological Characterization 122 of the Genus Hesperolinon 12. Appendix 3: Greenhouse Inoculations Involving H. breweri 132 13. Bibliography 140 iii Abstract Yuri P. Springer Epidemiology, Resistance Structure, and the Effects of Soil Calcium on a Serpentine Plant-Pathogen Interaction While the impacts of diseases in agricultural settings have long been appreciated, little is known about the role of plant pathogens in natural ecosystems. Studies that quantify the ecological impacts of diseases on wild plant populations, and link these impacts to resulting evolutionary patterns, inform our understanding of the dynamics of natural systems and allow theories about variation in the frequency, intensity, and outcome of antagonistic coevolution to be assessed. Plant communities associated with serpentine soils offer an intriguing setting in which to conduct such studies. While essentially nothing is known about the diseases of serpentine flora, evidence from agricultural systems suggests that low soil calcium levels typical of serpentine soils should make associated plants vulnerable to attack by pathogens. In contrast, an ecological theory attempting to explain patterns of edaphic endemism characteristic of serpentine plant communities posits that these low calcium soils may provide a refuge from disease. Studying the interaction between California dwarf flax, Hesperolinon californicum, and the rust fungus Melampsora lini, I tested these conflicting predictions and examined patterns of epidemiology and host resistance structure across the latitudinal range of the host species. Using a greenhouse experiment in which I manipulated the calcium concentration of serpentine soils I found that infection rates were lower for plants growing in higher calcium soils. This finding was supported by results of three years of epidemiological surveys conducted in sixteen wild H. californicum populations. Infection prevalence was positively correlated to host population latitude, altitude, and density, and negatively related to soil calcium concentration. Infection was associated with increased seedling mortality rates and reduced fecundity in adults. I documented a cline in infection, with high disease prevalence in northern plant populations decreasing steadily towards the south. A nearly identical pattern in host resistance structure was elucidated by greenhouse inoculations in which plants from each survey population were challenged with ten rust isolates. Genetic resistance was lowest in northern flax populations and increased gradually and continuously towards the south. This is one of a handful of studies that has investigated both epidemiological patterns and host resistance structure in a wild plant/pathogen interaction. Acknowledgements I am deeply indebted to many people who helped me overcome the countless scientific and personal challenges that presented themselves during the course of my dissertation research. First, I thank the three members of my thesis committee. Mark Carr offered me the chance to come to UCSC, granted me tremendous latitude to explore my intellectual curiosities, and maintained his good humor when I left the ocean for the “serpentine mountains.” Greg Gilbert was an exceptional mentor who shared his knowledge and passion for plant pathology, treated me with personal and professional respect, and exhibited tremendous tolerance of my often recalcitrant ways. Ingrid Parker connected me with Greg, and in addition to providing critical insights in matters of plant ecology and experimental design, helped me through early periods of personal uncertainty with indispensable pep talks. I thank each of them for their patience, sage guidance, encouragement, and confidence. I am also grateful to John Thompson, whose contagious enthusiasm for studies of coevolution and generous lab support helped get my thesis research started. Pete Raimondi was a source of clarity and valuable insight on scientific, bureaucratic, and personal quandaries, and was an invaluable advocate when I needed one. I received critical support in all aspects of data collection. The staff of the UC Davis DANR facility generously shared their soil analysis protocols with me, and Rob Franks at UCSC’s Institute of Marine Sciences trained me to use the requisite analytical equipment and to interpret data outputs. Collection and analyses of vi molecular data would have been impossible without the help of Martha Burford, Ammon Corl, Gwynne Corrigan, Katrina Dlugosch, Catherine Fernandez, Kate Horjus, Becky Hufft, Shawn Kuchta, Joshua McDill, Kate Mesa, Grant Pogson, Marina Ramon, and James Richardson. Brian Fullfrost and Jacob Pollock assisted me in my cartographic endeavors, and David Banghart provided computer expertise at critical moments. Jim Velzy taught me everything I know about plant husbandry, helped me develop protocols to germinate and grow my flax, and always made sure I was taken care of in the greenhouse. I thank Krikor Andonian, Dawn Jech, Haven Livingston, Ashleigh Lyman and my mom for assisting with data collection in the field and helping to keep the loneliness of fieldwork at bay. The botanical expertise of Joe Callizo, Susan Harrison, Neil McCarten, and Jake Ruygt steered me towards many flax populations I would never have discovered on my own. I also thank my Gilbert and Raimondi/Carr labmates, particularly postdocs Dave Lohse and Todd Minchinton, for their help in developing and focusing my research ideas. I was very fortunate to receive wonderful accommodations while away from Santa Cruz during my field seasons. Joe Callizo shared his home with me at the Wantrup Wildlife Refuge in Pope Valley. His insatiable hunger for knowledge, incredible memory, and desire to share his insights and experiences made Joe a priceless botanical advisor and a wonderful companion. Paul Ainger and Cathy Koehler at the UC Davis Ray Krauss Field Station were Joe’s Lake Country counterparts, making sure I was well taken care of during my work at and around the McLaughlin Reserve. During forays in the east bay I was treated to unparalleled vii hospitality by Kord and Van Kober in Berkeley and Scotty and Shae Kober in San Francisco. The study described in Chapter 1 was performed as part of a senior thesis research project bravely undertaken by Bree Hardcastle. Bree did an exceptional job, showing tremendous ingenuity, independence, and diligence in executing an experiment that presented a variety of logistic challenges. In the face of many obstacles, including my shortcomings as a mentor, she maintained her upbeat attitude, meticulous methodology, and commitment to the project. She has the makings of a great ecologist, and I sincerely hope that her participation in this research motivated her to continue her scientific training. It is largely due to the support of many dear friends that I managed to reach the light at the end of the proverbial tunnel. When I was beset by frustration or doubt, their words of advice and encouragement got me back on track, and they provided many pleasant distractions from the stresses of graduate student life. My most sincere thanks to Holly Alpert, Arnold Ammann, Krikor Andonian, Jeff Barna, Rachel Barnett-Johnson, Martha Burford, Kathy Chanpong, Tish Conway-Cranos, Gwynne Corrigan, Galen Crippin, Jared Figurski, Melissa Foley, Julio Harvey, Cynthia Hays, Kate Horjus, Becky Hufft, Matt Kaufman, Kord, Van, and Scotty Kober, Carolyn Kurle, Bruce Lyon, Jack Malone, Todd Minchinton, Marisa Mitchell, Kelley O’Neill, Brian Ort, Debi Pian, Marina Ramon, Mark Readdie, Diana Stellar, Chris and April Tritto, and Shaye Wolf. In particular I would like to acknowledge the unwavering support and incredible friendship of Ryan Calsbeek, Nicole Ikkanda, Marie Waszak, viii and Megan Williams. Thanks also to my many friends at the Bike Church and the Santa Cruz Paddleboard Union for providing memorable diversions from my scientific pursuits. I gratefully acknowledge the generous financial assistance provided by the following organizations in support of my dissertation research: the UC Davis Genetic Resources Conservation Program, the UC Santa Cruz STEPS Institute, the California Native Plant Society (state level and east bay
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