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Systematics of Penstemon Section Ericopsis (Plantaginaceae), a Group of Plant Species Native to the Intermountain West

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Systematics of Penstemon Section Ericopsis (Plantaginaceae), a Group of Plant Species Native to the Intermountain West Systematics of Penstemon section Ericopsis (Plantaginaceae), a group of plant species native to the Intermountain West DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Aaron James Wenzel Graduate Program in Evolution, Ecology and Organismal Biology The Ohio State University 2016 Dissertation Committee: Andrea Wolfe (Advisor) John Freudenstein Laura Kubatko Steve Matthews Copyrighted by Aaron James Wenzel 2016 Abstract Penstemon Mitchell (Plantaginaceae) is the largest plant genus endemic to North America with approximately 283 species. Most species are only relatively recently diverged from one another, which has left questions about taxonomy and systematics in Penstemon unanswered. This dissertation considered one section in the genus, Ericopsis Keck, a group of 15 species from the Intermountain Region in western USA. Evolutionary and ecological frameworks were used to investigate phylogenetic relationships, population demographic history, polyploidy, and niche divergence. Chapter 1 presents the results of a phylogenetic study of section Ericopsis. Using a total of 39 nuclear and chloroplast loci obtained from high-throughput targeted sequencing and Sanger sequencing, the exact membership of section Ericopsis was able to be determined. This included two taxa not currently classified in section Ericopsis, P. pinifolius and P. dolius var. dolius. It was also determined that three current Ericopsis species, P. acaulis, P. yampaensis, and P. laricifolius, group in a clade with species from section Cristati with high support. Within the Ericopsis clade, however, nodal support for relationships among species was low, so strong conclusions about exact relationships are difficult to ascertain. There was support for a clade comprising the species of subsection Linarioides, as well as groups consisting of the varieties of P. caespitosus and P. crandallii. It is likely that incomplete lineage sorting and hybridization are causing ii gene tree incongruence in these analyses, which may be alleviated by adding additional sequence data from informative loci. Chapter 1 also provides the context for questions asked in subsequent chapters of the dissertation. Chapters 2 and 3 use a population genetics framework to study evolutionary dynamics in two widespread species from section Ericopsis. In chapter 2 the variable P. linarioides Gray is considered. This population genetics study included 299 individuals from 22 populations (representing four of the five varieties) and seven microsatellite loci. Overall genetic structure was limited, with the majority of genetic variation distributed within individuals. However, clustering methods revealed that populations of the same varieties grouped with one another, and that varieties linarioides and coloradoensis share a close relationship. In addition there was evidence of hypothesized cryptic diversity within var. sileri, with populations forming three distinct clusters, representing the Markagunt Plateau of southern Utah, the Beaver Dam/Bull Valley mountains of southern Utah, and the Kaibab Plateau of northern Arizona. Finally, an historical demographic study using approximate Bayesian computation found that a lineage most likely diverged from var. sileri and then split again into varieties linarioides and coloradoensis. The timing of this event is estimated to be around the end of the Pleistocene. Chapter 3 is a population genetics study of P. caespitosus Nutt. ex. Gray, a species with three varieties from Utah, northern Arizona, and western Colorado. Penstemon caespitosus is an interesting case study because one of its varieties, desertipicti, is a tetraploid while varieties caespitosus and perbrevis are diploid. A total of 222 individuals from nine populations were considered in this study with the same iii microsatellite loci from chapter 2. Genetic structure was much greater in P. caespitosus than in P. linarioides. Results from clustering analyses revealed a close relationship between var. perbrevis (from central Utah) and var. desertipicti (from southwest Utah and northern Arizona). Tetraploid var. desertipicti also contained many unique alleles, consistent with a pattern of allotetraploidy. Although one of the parent progenitors is likely var. perbrevis, the other parent is most likely another species from section Ericopsis that shares a close geographic range with var. desertipicti (such as P. thompsoniae or a variety of P. linarioides). Chapter 4 builds on the results of the first three chapters by exploring niche divergence between sister taxa using ecological niche modeling (ENM). ENMs were constructed in MaxEnt using presence-only data collected from herbarium records. A total of four comparisons were made between sister species and varieties. Most comparisons showed a situation of incomplete niche divergence, where niches of sister taxa were similar but not identical to one another. The comparisons made between varieties of P. laricifolius (laricifolius vs. exilifolius) and varieties of P. linarioides (linarioides vs. coloradoensis) revealed that the two niches were more different than would be expected at random. The largest amount of niche divergence was between diploid P. caespitosus var. perbrevis and tetraploid var. desertipicti. These results support a scenario where sister taxa are diverging along environmental gradients (mostly precipitation and temperature during certain times of the year), and where polyploidy has led to even greater niche divergence. iv Dedication I dedicate this dissertation to my wife and parents, who have provided me with unconditional love and support as I have taught, worked in the lab, and chased after plants in the field for weeks at a time. Special thanks are in order for Beth and Mark Wenzel, who have always encouraged my academic endeavors and have especially supported me throughout graduate school. I offer special thanks as well to the love of my life, Naomi McDowell. Your support of my passion for the natural world has been immeasurable, and I am so happy to have had you as a partner throughout all of this. v Acknowledgments This work would not have been possible without the input and assistance of many individuals, and I am indebted to all who have taken the time to help me these past six years. I would first like to express my gratitude to Andrea Wolfe, my advisor, for mentoring me from a naïve first-year grad student to PhD graduate. Your guidance and support has been immeasurable. I would also like to thank past mentors I have had. Janet Gehring (Bradley University), my first research advisor, introduced me to plant population genetics and piqued my interest in the broader field of evolutionary biology. I am also thankful to my mentors at my alma mater Xavier University, especially Dorothy Engle and Jen Robbins. Your guidance during the formative years of my scientific education was invaluable and unforgettable. I am thankful to all who helped me in the field and made collections for me, including Marc Baker, Mike Stevens, Marcel Jouse, Frank Riechenbacher, Miriam Islam, and Al Schneider. I am also thankful to my fellow graduate students who took time help me with issues and read countless drafts of grant proposals and manuscripts: Sam Herrmann, Tony Fries, Jimmy Chiucchi, Mike Sovic, Ryan Folk, And Eric McCluskey. I appreciate all of the help and advice I have received from my committee members, as well as help from Jose Diaz, our lab technician. Finally, thank you to all of my fellow vi comrades in the Wolfe Pack, especially Dan Robarts and Paul Blischak. Whether it was giving advice on how to resolve a certain issue in the lab, explaining a new statistical analysis, or providing company during a late night lab session, both of your friendships have been enriching to me scientifically and personally. vii Vita June 2006 .......................................................Vandalia-Butler High School May 2010 .......................................................B.S. Biology, Xavier University 2010 to present ..............................................Graduate Teaching Associate, Department of Evolution, Ecology, and Organismal Biology, The Ohio State University Publications Wenzel, A. (2015). Systematics of Penstemon section Ericopsis. Bulletin of the American Penstemon Society, 74: 9-21. Blischak, P.D., Wenzel, A.W., and Wolfe, A.D. 2014. Gene Prediction and Annotation in Penstemon (Plantaginaceae): A Workflow for Marker Development from Extremely Low-Coverage Genome Sequencing. Applications in Plant Sciences 2 (12), http://dx.doi.org/10.3732/apps.1400044. Fields of Study Major Field: Evolution, Ecology and Organismal Biology viii Table of Contents Abstract ............................................................................................................................... ii Dedication ........................................................................................................................... v Acknowledgments.............................................................................................................. vi Vita ................................................................................................................................... viii Publications ...................................................................................................................... viii Fields of Study ................................................................................................................
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