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Systematics, Phylogeography, Fungal Associations, and Photosynthesis

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Systematics, Phylogeography, Fungal Associations, and Photosynthesis Systematics, Phylogeography, Fungal Associations, and Photosynthesis Gene Evolution in the Fully Mycoheterotrophic Corallorhiza striata Species Complex (Orchidaceae: Epidendroideae) Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of the Ohio State University By Craig Francis Barrett, M. S. Evolution, Ecology, and Organismal Biology ***** The Ohio State University 2010 Dissertation Committee: Dr. John V. Freudenstein, Advisor Dr. John W. Wenzel Dr. Andrea D. Wolfe Copyright by Craig Francis Barrett 2010 ABSTRACT Corallorhiza is a genus of obligately mycoheterotrophic (fungus-eating) orchids that presents a unique opportunity to study phylogeography, taxonomy, fungal host specificity, and photosynthesis gene evolution. The photosysnthesis gene rbcL was sequenced for nearly all members of the genus Corallorhiza; evidence for pseudogene formation was found in both the C. striata and C. maculata complexes, suggesting multiple independent transitions to complete heterotrophy. Corallorhiza may serve as an exemplary system in which to study the plastid genomic consequences of full mycoheterotrophy due to relaxed selection on photosynthetic apparatus. Corallorhiza striata is a highly variable species complex distributed from Mexico to Canada. In an investigation of molecular and morphological variation, four plastid DNA clades were identified, displaying statistically significant differences in floral morphology. The biogeography of C. striata is more complex than previously hypothesized, with two main plastid lineages present in both Mexico and northern North America. These findings add to a growing body of phylogeographic data on organisms sharing this common distribution. To investigate fungal host specificity in the C. striata complex, I sequenced plastid DNA for orchids and nuclear DNA for fungi (n=107 individuals), and found that ii the four plastid clades associate with divergent sets of ectomycorrhizal fungi; all within a single, variable species, Tomentella fuscocinerea. Furthermore, the Californian plastid clade showed extreme sub-specificity toward a single Tomentella clade across multiple populations. This is perhaps the most extensive investigation of specificity for any mycoheterotroph, and has conservation implications for these rare orchids. To address taxonomy, conservation, and phylogeography within the C. striata complex, I analyzed continuous floral characters, plastid DNA, and nuclear DNA for 155 individuals across North America. The main finding was that C. striata, C. bentleyi, and C. involuta are separate species. Within the widespread, variable C. striata, there are three evolutionarily significant units, which I recognize as varieties; these findings carry further conservation implications for C. striata. Phylogeographic breaks in C. striata are similar to those in several co-distributed ectomycorrhizal tree species, suggesting these species may have responded similarly to past geologic/climatic processes, but the timing of these events in C. striata remains to be addressed. iii Dedicated to my friends and loved ones, to all the great educators who have endeavored to make me a better biologist and a better person, and to all who understand and strive to defend the importance of science and good science education. iv ACKNOWLEDGEMENTS I would like to thank my Ph.D. committee for their support over the last six years. First, I thank my adviser John Freudenstein for the hours of dedicated work he has put into making me a better scientist. Whether teaching classes, reviewing our manuscripts, having conversations at the lunch table, or updating me on the finer points of espresso making while in the car during collecting trips, John has invested a lot in me; I appreciate it and will never forget it. I thank Dr. John Wenzel for his advice and help along the way, but especially for the thought provoking conversations that occurred nearly every day; also for crawfish and campfire parties at his house. I thank Dr. Andi Wolfe for feedback on manuscripts and for challenging me to become a better researcher. I thank Dr. Kobi Abdul-Salim for numerous informative conversations on research, software, and teaching. I thank Dr. Meg Daly for advice, support, and chocolate pie. Although Meg was not one of my committee members, she has gone above and beyond the call of duty in helping me over the past few years. I thank Dr. Lisle Gibbs for manuscript feedback, and for organizing extremely helpful seminars in population genetics research methods over the past few years (along with Dr. Laura Kubatko and Dr. Paul Fuerst). I would like to thank everyone at the Museum who participated in the Phylogenetics Discussion v Group over the past six years—this has been one of the most important factors in my development as a systematist. I thank Dr. Lee Taylor (UAlaska-Fairbanks) for numerous fungus and coevolution related discussions, for his feedback on manuscripts, and for inviting me to coauthor a book chapter on mycoheterotroph population genetics. I thank Urmas Kõljalg and Kessy Abarenkov (University of Tartu, Estonia) for assistance with the UNITE fungal ITS sequence database, and for help with writing a manuscript now published in American Journal of Botany. I thank Heather Stephens for her patience, support, love, and willingness to engage in nerdy conversations about everything from statistics to botany to economics. She has also been a wonderful field coworker for the past three years, with many more to come! I thank my family and friends for their continued love and support, and willingness to understand my motivation for moving to Ohio for six years. To my parents, Kathy and Frank, and to my sister Jana, thanks for supporting me during both good and bad times, and encouraging me to see this through to the end. I thank the following for their assistance in collecting plant material: Michael Burzynski (NL, Canada), Diana Jolles (CA, OR), Lorne Heshka (MB, Canada), Josh Horky (MN/WI), K. Inoue (Japan), and John Maunder (NL, Canada). I would like to especially thank Gerardo Salazar (UNAM, Mexico), for assistance with fieldwork in Mexico, and especially for driving around Mexico City, which otherwise would have been a daunting task. vi For discussion, feedback, and invaluable assistance, I thank Gale Azcarraga- Carter, Stan Bentley, Mike Broe, Sibyl Bucheli, Ryan Caesar, Brian Chaplin, Ron Coleman, Meg Daly, Cynthia Dassler, Jose Díaz (a huge thanks for assistance with DNA sequencing), Cathy Drake, Charles Garratt, Lisle Gibbs, Luciana Gusmao, Faith Haleem, Tim Hartley, Diana Jolles, Aaron Kennedy, Shawn Krosnick, Laura Kubatko, Annie Lindgren, Paul Manos, John Maunder, Jeff Morawetz, Joe Raczkowski, Chris Randle, Abby Reft, Jeff Rose, Erik Rothacker, Donna Schenk, Brandon Sinn, Mesfin Tadesse, Charuwat Taekul, Elijah Talamas, Alejandro Valerio, Earvin Washington, John Wenzel, Andi Wolfe, and Matt Yoder. Thanks to Martin Bidartondo, Mark Simmons, and Neil Snow for comments on various manuscripts. For permission to collect plants, I thank Frank Duran, Don Golnick, Dave Harris, Andy Kratz, Teresa Prendusi, Art Fong, Keith Tignor (for the endangered Corallorhiza bentleyi), Joe Brazil, USDA, ParksCanada, and the Canadian Forest Service. Funding was provided by the American Orchid Society, the American Society of Plant Taxonomists, OSU Herbarium Janice Carson Beatley Fund, OSU Office of International Affairs Dissertation Travel Grant, OSU Council of Graduate Students Edward J. Ray Award, and National Science Foundation Grant DEB-0415920. vii VITA December 27, 1979………………………………………………Born - Ilion, NY, USA 2002……………………………………….B.A., Hartwick College, Oneonta, NY, USA 2004……………………………….M.S., SUNY - Binghamton, Binghamton, NY, USA 2004-2010……………….Graduate Teaching Assistant, OSU Presidential Fellow, Ohio State University, Columbus, OH, USA PUBLICATIONS 1. Barrett, C. F., Freudenstein, J. V., Taylor, D. L., and U. Kõljalg. 2010. Rangewide analysis of fungal associations in the fully mycoheterotrophic Corallorhiza striata complex (Orchidaceae) reveals extreme specificity on ectomycorrhizal Tomentella (Thelephoraceae) across North America. American Journal of Botany 97: 628-643. 2. Freudenstein, J. V. and C. F. Barrett. 2010. Mycoheterotrophy and diversity in Orchidaceae with a focus on Corallorhiza. In: Proceedings of the Fourth International Conference on the Biology of the Monocotyledons. Seberg, O., Petersen, G., Barfod, A. S., and J. I. Davis, eds. Aarhus University Press, Copenhagen, Denmark. 3. Barrett, C. F. and J. V. Freudenstein. 2009. Patterns of morphological and plastid DNA variation in the Corallorhiza striata species complex (Orchidaceae, Epidendroideae). Systematic Botany 34: 496-504. 4. Barrett, C. F. and J. V. Freudenstein. 2008. Molecular evolution of rbcL in the mycoheterotrophic Coralroot orchids (Corallorhiza Gagnebin: Orchidaceae). Molecular Phylogenetics and Evolution 47: 665-679. viii 5. Barrett, C. F. and M. A. Parker. 2006. Coexistence of Burkholderia, Cupriavidus [Ralstonia], and Rhizobium sp. nodule bacteria on two native Mimosa spp. from central Pacific Costa Rica. Applied and Environmental Microbiology 72: 1198-1206. 6. Barrett, C. F. and M. A. Parker. 2005. Prevalence of Burkholderia sp. nodule symbionts on four mimosoid legumes from Barro Colorado Island, Panama. Systematic and Applied Microbiology 28: 57-65. FIELDS OF STUDY Major Field: Evolution, Ecology, and Organismal Biology Area of Emphasis: Systematics and Evolution ix TABLE OF
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