Do ecological communities co-diversify? An investigation into the Sarracenia alata pitcher plant system DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in the Graduate School of The Ohio State University By Jordan David Satler Graduate Program in Evolution, Ecology, and Organismal Biology The Ohio State University 2016 Dissertation Committee: Dr. Bryan Carstens, Advisor Dr. Laura Kubatko Dr. John Freudenstein Copyright by Jordan David Satler 2016 Abstract Interactions among species are driving forces behind the formation, structure, and persistence of ecological communities. The nature of species interactions that characterize communities, however, has long been debated by ecologists, varying from communities as fluid entities to communities as evolving units. For species with obligate interactions (e.g., host and parasite, plant and pollinator), we might expect these ecologically dependent associations to be reflected in a shared evolutionary history, yet relatively few studies have demonstrated this process in nature. To address this central tenet in ecology and evolutionary biology, my research explores co-diversification in the Sarracenia alata pitcher plant system. Sarracenia alata (family Sarraceniaceae) is a carnivorous pitcher plant distributed along the Gulf Coast of the American southeast, bisected by the Mississippi River. Leaves of this plant are tube-shaped and filled with fluid, adapted for the capture and digestion of prey items. The breakdown of prey provides inorganic compounds to the plant, necessary in the nutrient-poor habitats where these plants are found. In addition to prey capture, the plant’s modified leaves harbor a unique biota of associated organisms (i.e., inquilines)—diverse species that share ecological relationships and often provide important services (e.g., secrete digestive enzymes) for the plant. My dissertation tests coevolution theory, exploring how a host ii plant may influence the population genetic structure of associated species. Shared structure would suggest stable ecological relationships through evolutionary time, and would provide evidence that ecologically interacting lineages can evolve as a unit. I first analyzed DNA sampled directly from the pitcher fluid to identify microorganisms contained within the community (Chapter 2). My results recover a diverse set of taxa found within the pitcher fluid, and demonstrate that roughly half of the small eukaryotes (e.g., fungi, mites) share population genetic structure with S. alata, suggesting a shared evolutionary history among these interacting species. I further explored these questions of co-diversification with six arthropod species (insects and arachnids) that interact with the host plant; these species range on the ecological spectrum from obligate symbionts to opportunistic predators (Chapter 3). I first developed a novel method for quantifying phylogeographic congruence (Phylogeographic Concordance Factors; PCFs). Results show ecological association correlates with a shared evolutionary history, and suggests that multiple arthropods co-diversified with the host pitcher plant. I then tested for simultaneous divergence across the Mississippi River, an important biogeographic barrier in this region, by estimating population splitting times in five arthropods spanning this barrier (Chapter 4). Results suggest that two of the arthropods dispersed across the Mississippi River (from east to west) synchronously with the plant. A third arthropod displays similar population genetic patterns as the plant, but is estimated to have dispersed across the Mississippi River at a later time. My dissertation provides evidence for the evolutionary stability of interacting lineages, suggesting that ecological communities co-diversify. iii This dissertation is dedicated to my parents, June and Larry Satler, for their love, support, and encouragement as I pursued my interests. iv Acknowledgments First and foremost, I would like to thank my advisor, Dr. Bryan Carstens, for being an outstanding mentor as I pursued my PhD. Bryan has been a wonderful advisor, and has helped me grow as a biologist and as a person. I have appreciated Bryan’s time and efforts with me, and his willingness to listen to my ideas, provide constructive criticism, and to help clarify concepts when they didn’t quite make sense. Bryan has also been incredibly patient and understanding with me, and I am tremendously thankful for that. I feel fortunate to have had Bryan as a PhD advisor. I would also like to thank my other committee members, Dr. Laura Kubatko and Dr. John Freudenstein, for their helpful comments, suggestions, and discussion over the years, and for providing their time towards this process. In particular, I would like to thank Dr. Laura Kubatko for her fantastic seminars each spring, covering topics I am eager to learn and discuss and in explaining difficult concepts in a way to make them understandable. These seminars have been instrumental in my growth as a scientist. In addition, I would like to thank Dr. Norm Johnson for being a valuable member of my candidacy committee. I appreciated Norm’s questions and comments during this time, and in our discussions over the years. I would like to thank my funding sources for making much of my project possible. Specifically, I would like to thank the National Science Foundation (Doctoral v Dissertation Improvement Grant DEB-1501474), the Ohio State University (Presidential Fellowship), the Society for the Study of Evolution (Rosemary Grant Award for Graduate Student Research), and the Society of Systematic Biologists (Graduate Student Research Award). I would also like to thank Dr. Marshal Hedin, Dr. Robb Brumfield, and Dr. Frank Burbrink for writing letters of recommendation for me for the Presidential Fellowship. The bulk of my analyses were carried out on the Oakley cluster at the Ohio Supercomputer Center and the Ohio Biodiversity Conservation Partnership (OBCP) Informatics Infrastructure housed at the Museum of Biological Diversity. These two computing resources were fantastic. In addition, I would like to thank Joe Cora, who was an excellent resource when I had questions or needed assistance with the OBCP cluster. I have been fortunate to have had many wonderful lab mates during my PhD. I would like to thank current students Ariadna Morales-Garcia, Megan Smith, Sergei Soloneko, and Greg Wheeler, for excellent discussion and interactions over the years. I have thoroughly enjoyed our lab meetings and discussions of papers and ideas. I’m excited to see where their paths go during their academic careers! It’s crucial for me to thank the Carsten lab members present when I first entered the lab, Sarah Hird, John McVay, Tara Pelletier, and Noah Reid. My first year in the lab was incredible, and I have many wonderful memories of our time together at Louisiana State University. A big reason for me initially joining Bryan’s lab was because of these four people, and I know I made the right decision and greatly value the time we had together. In addition, Danielle Fuselier was a superstar undergraduate in the lab at LSU, and helped with both field work and lab work during my first year. I would like to thank Michael Gruenstaeudl for great vi discussion and help with computer coding while he was a postdoc in the lab at Ohio State. I would also like to thank Matt Demarest and Maxim Kim for help and assistance regarding computer coding for data analysis while they worked in the lab my first couple of years at Ohio State. So many people have helped contribute to where I am today in my academic career; there are too many to thank but I will give it my best shot! First, I would like to thank my Master’s advisor, Dr. Marshal Hedin. Marshal was instrumental in getting me started with research, and in learning how to be a scientist. I wouldn’t be where I am today without Marshal’s guidance and tutelage, and am forever thankful that as an undergraduate at San Diego State University, I enrolled in a course called Terrestrial Arthropod Biology. That class changed my life. I would like to thank the many faculty and graduate students at LSU that I interacted with during the first year of my PhD. I had many wonderful discussions pertaining to science and life during this time, and look back fondly on those conversations and experiences. I would also like to thank the many faculty and graduate students at Ohio State. These past four years have been very important in my life, and the interactions, discussions, and experiences with these wonderful people has made it a time I will never forget. I am hesitant to list names for concern I may leave someone out, but I have forged many strong friendships over these past few years, and those people know who they are. Academia is a gift and a curse in that we get the opportunity to meet such wonderful people, but many of our stays are fleeting in time. I’m thankful for all the wonderful relationships I’ve had over the years at vii Ohio State, and look forward to continuing our friendships as we move forward in our careers. I would like to thank Greg Dahlem and Rob Naczi for help with the identification of flesh flies in my study. I would like to thank Maggie Koopman and Amanda Zellmer for data collection and analysis pertaining to Chapter 2, and for their roles in the earlier work on Sarracenia alata building a foundation for the system with which I could explore with the arthropods. I would like to thank Kelly Zamudio, the Zamudio lab, and Steve Bogdanowicz for assistance with RAD sequencing. I would also like to thank Mike Sovic for discussion regarding RAD sequencing and protocols, and various aspects of the analysis of RAD data. Finally, I would like to thank my family, friends, and those closest to me for their love, support, and encouragement over the years as I pursued my PhD. Lisa Miller has been a wonderful girlfriend and companion the past couple years, and has provided much needed relief to get my mind off work and explore nature and the many wonderful things life has to offer.
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