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THE GENETIC STRUCTURE OF SPECIES’ GEOGRAPHIC RANGES: AN EVALUATION USING THE COSTAL DUNE ENDEMIC CAMISSONIOPSIS CHEIRANTHIFOLIA (ONAGRACEAE) By Adriana López Villalobos A thesis submitted to the Department of Biology in conformity with the requirements for the Degree of Doctor of Philosophy Queen’s University Kingston, Ontario Canada June 2017 Copyright © Adriana López-Villalobos, 2017 ABSTRACT The development of molecular techniques has spurred thousands of population genetic studies on a wide variety of plant and animal species. Particularly important, but still relatively rare, are studies that properly test for geographic variation in genetic structure across species’ ranges. This thesis investigates the effects of population density, mating system variation, distance between populations and hybridization on the genetic diversity, differentiation and structure across the range of Camissoniopsis cheiranthifolia (Onagraceae). By combining a transplant experiment with microsatellites, I also provide an empirical test of one of the most poorly resolved questions in evolutionary biology: Why do species exhibit limits to their distributions? I developed 24 species-specific nuclear microsatellites loci (nSSR) and used 13 of these and six variable chloroplast microsatellites (cpSSR) to investigate the genetic consequences of the transition from outcrossing to selfing in C. cheiranthifolia. As predicted, small-flowered, selfing populations had lower nSSR diversity (but not cpSSR) than large-flowered, outcrossing populations but they were not more differentiated. The reduction in diversity was greater than the expected from selfing alone, but could not be accounted for by indirect effects of selfing on population density. Five parapatric nSSR clusters and three groups of cpSSR haplotypes usually (but not always) differed in mating system, suggesting that selfing may often initiate ecogeographic isolation. However, lineage-wide diversity failed to support that selection for reproductive assurance initiated selfing in this species. I also investigated if hybridization with C. bistorta has influenced the genetic structure of C. cheiranthifolia in areas of closest parapatry. I confirmed that closet parapatry was associated with extensive genetic continuity between self-incompatible C. cheiranthifolia and C. bistorta ii and these were indistinguishable genetically within the broader context of geographic variation in C. cheiranthifolia, suggesting that C. bistorta could be an inland ecotype of C. cheiranthifolia Finally, fitness increased toward and beyond the northern range limit of C. cheiranthifolia but edge individuals were not best suited to conditions beyond the range. Despite strong genetic differentiation and very low, nondirectional gene flow, there was no evidence of local adaptation, except at the coarsest spatial scale, suggesting range limitation via constraints to dispersal. iii Co-Authorship My thesis has been prepared in the manuscript format as outlined in the guidelines provided by The School of Graduate Studies. All chapters are co-authored by Dr. Christopher G. Eckert, who contributed financially and intellectually to the design, development and editing of the thesis. Karen E. Samis collaborated in two of the manuscripts presented in this thesis. In chapter one she constructed the genetic library used to develop the microsatellite markers used in the first and subsequent chapters. In chapter 5 she conducted the transplant experiment, collected and analyzed these data and contributed at all stages of the manuscript preparation. PUBLICATIONS ARISING FROM AND INCLUDED IN THIS THESIS Lopez-Villalobos A., Samis, K. E. and Eckert, C.G. 2014. Microsatellite primers for Camissoniopsis cheiranthifolia (Onagraceae) and cross-amplification in closely related species. Applications in Plant Sciences 109: 599–611. López-Villalobos A. and Eckert, C.G. (submitted 16 Nov. 2016). Consequences of multiple mating system shifts for population and range-wide genetic structure in a coastal dune plant. Molecular Ecology. López-Villalobos A. and Eckert, C.G. (in prep.). Does hybridization contribute to range-wide population genetic structure in a coastal dune plant? For submission to American Journal of Botany. Samis, K.E., A. López-Villalobos, and C.G. Eckert. 2016. Strong genetic differentiation but not local adaptation toward the range limit of a coastal dune plant. Evolution 70: 2520–2536. iv OTHER PUBLICATIONS ARISING FROM, BUT NOT INCLUDED IN THIS THESIS: Dick, C.A., J.A. Herman, R.E. O’Dell, A. Lopez-Villalobos, C. Eckert, and J.B. Whittall. 2013. Cryptic genetic subdivision in the San Benito evening primrose (Camissonia benitensis). Conservation Genetics 15: 165–175. Viengkone J., López-Villalobos A., & Eckert, C.G. (in prep.). A test of whether local genetic stocks yield better restored populations in a Pacific coastal dune endemic plant. v ACKNOWLEDGEMENTS First and foremost, I would like to thank my supervisor Chris Eckert for his time and effort spent reading and providing feedback on my chapters. I want to acknowledge his patience throughout this long journey for both of us. Thank you as well for helping me improve my thinking, research and writing skills. I also want to thank each one of my committee members Drs. Vicki Friesen, Steve Lougheed, and Ryan Danby for their availability, support and their valuable comments to this project. Special thanks to Karen Samis for all the information provided, the guidance and support, I received, especially at the beginning of my PhD. Thank you for being such a great team member and collaborator. I thank the CONACYT (The Mexican National Council for Science and Technology) for funding this doctoral degree at Queen's University and the Natural Sciences and Engineering Council of Canada (NSERC) for the Discovery Grants to CGE who contributed to the expenses of this research. The work collated in this thesis is the product of between two and three-month field seasons and at least three years of lab work worth of data. It involved thousands of DNA extractions, agarose gels, PCR reactions, fragment sequenced, tons of frustration but lots of amazing students without whom this would not have been possible. I am very grateful to my field crew: Lindsey Button, Natalie Morril, Karen Samis and Anna Hargreves. To my image analyses team: Han Tao, Carlie Smith, Amanda Yuan and Moumita Kramar. And the best lab crew ever: Benjamin Shiff, Kyle Millar, Jon Vienkone and Meera Manghani. I would like to extend a special recognition to Zhengxin Sun for all his hard work in producing my thousands of PCR vi fragments, for his guidance, his help troubleshooting and the encouragement I received from him throughout the entire phase of my lab work. I want to thank many good-natured people that marked my PhD with their generosity and friendship in one way or another during my field trips. Mary Alice Kesler, Sula Vanderplank, Eli Wehncke, Javier “el Twinky”, Alicia Cardoso, Rodrigo Beas, Sara Teck, Julio Lorda, Dave Hubbard and Jenny Dougan for providing me with a place to land in different parts along the coast of Baja California and California. Jon Rebman, Mike Simpson, Jose Delgadillo and Sula for their advice id-ing the difficult camissonias during field collections, for showing me the beauty of the Baja California Flora and for allowing me to use the herbarium facilities at SDNHM and Rancho Santa Ana Botanical Garden. Many thanks go to all the past and present lab mates at the Eckert lab. For our science and non-science conversations, for their support and invaluable companionship during this time. Thanks to friends and colleagues at the Biology Department for those special times. Special thanks to go to Maggie Barkowska for helping me with coding complicated R functions, for encouraging me to talk out loud my results and help me brainstorm ideas, for the support and friendship I recieved in this last stage of my PhD. Further, I would like to thank everybody close to me outside of the Biology Department, the support and community at the BRC, my family and friends here in Kingston, in Portugal and back in the Mexico. Lulú, Rubén y Alex gracias por no tirar la toalla, por su amor y apoyo incondicional en todo momento. No hay palabras para expresar mi infinito agradecimiento. Ao Nuno Ramalho por tudo isso e muito mais. Obrigada por todo o teu apoio agora e até sempre. vii TABLE OF CONTENTS ABSTRACT ................................................................................................................................. ii CO-AUTHORSHIP .................................................................................................................... iv Publications arising from and included in this thesis: .................................................................. iv Publications arising from, but not included in this thesis: ............................................................. v ACKNOWLEDGEMENTS ....................................................................................................... vi TABLE OF CONTENTS ......................................................................................................... viii LIST OF TABLES ..................................................................................................................... xii LIST OF FIGURES ................................................................................................................... xv LIST OF ABREVIATIONS.....................................................................................................
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  • Plant Curiosities

    Plant Curiosities

    ROOTS OF SCIENTIFIC NAMES PLANT CURIOSITIES What do those cryptic scientific names mean? Before starting with the plant list, here are some names that occur in multiple species, so the details are put here and will not be repeated later. Names derived from people fremontii After John Charles Frémont (1813–1890), the “Pathfinder.” Frémont was an Army officer, a senator representing the new state of California in 1850, and in 1856 a presidential candidate of the anti-slavery Republican Party. Apparently, he was also an avid and prolific plant collector on his four expeditions to the American West in the 1840s. nuttallii, nuttallianus, nuttallianum, nuttalliana After Thomas Nuttall (1786–1859), an English botanist and ornithologist who explored America from 1808 to 1841. parryi, parryii After Dr. Charles Christopher Parry (1823–1890), who, of course, named the Torrey Pine and the Chaparral Yucca, among numerous other plants that actually bear his name. Names related to places californica, californicus, californicum: California Suffixes meaning flowers -anthos, -anthus, from the Greek anthos, blossom -florum, -flora, from the Latin flos Suffixes meaning grasses -chloa, possibly from Greek, in which chloros is greenish Suffixes meaning leaves -folium, -folia, from the Latin word folium -phyllum, -phylla, from the Greek word phyllon Prefixes and names for specific features edulis-, edible; from the Latin edere, eat dumosum, dumosa, bushy, shrubby; from the Latin dumus, thorny bush 1 Eri-, Erio-, hairy or woolly; from the Greek erion fasciculata,