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REPRODUCTIVE ECOLOGY and GENETICS of PLANT INVASIONS: a CASE STUDY of LYTHRUM SALICARIA (PURPLE LOOSESTRIFE) by Christopher M. B

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REPRODUCTIVE ECOLOGY and GENETICS of PLANT INVASIONS: a CASE STUDY of LYTHRUM SALICARIA (PURPLE LOOSESTRIFE) by Christopher M. B REPRODUCTIVE ECOLOGY AND GENETICS OF PLANT INVASIONS: A CASE STUDY OF LYTHRUM SALICARIA (PURPLE LOOSESTRIFE) by Christopher M. Balogh A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto © Copyright by Christopher M. Balogh 2018 REPRODUCTIVE ECOLOGY AND GENETICS OF PLANT INVASIONS: A CASE STUDY OF LYTHRUM SALICARIA (PURPLE LOOSESTRIFE) Christopher M. Balogh Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto 2018 ABSTRACT Biological invasions provide a valuable context for studying contemporary evolution. Because reproduction is a key process determining invasion success, investigations of the reproductive ecology and genetics of populations are particularly insightful. My Ph.D. thesis is comprised of five inter-related studies on Lythrum salicaria (purple loosestrife), a tristylous plant from Eurasia that has invaded wetlands in North America during the past 150 years. The specific questions I addressed, using computer simulations, surveys of natural populations, and glasshouse and field experiments, concerned the mechanisms governing the frequencies of mating types in populations, the characteristics and functional significance of partial self-incompatibility, the influence of floral morph structure and demography on mating and fertility, and the occurrence and significance of inbreeding depression for invading populations. ii Stochastic computer models incorporating morph-specific self-compatibility and tetrasomic inheritance revealed patterns of morph-frequency variation and asymmetric morph loss consistent with data from L. salicaria, including a survey I conducted in Ontario of 114 populations that revealed stochastic loss of the S-morph from small populations. Glasshouse experiments involving controlled self- and cross-pollination demonstrated that ~34% of L. salicaria plants exhibited partial self-incompatibility, that this trait was weakly heritable, and was stable in expression over two years. Progeny testing of open-pollinated families in six populations and isolated plants in a field experiment revealed high rates of inter-morph mating demonstrating that L. salicaria is robust to demographic variation associated with colonization. Cumulative estimates of inbreeding depression (δ) in a four-year experiment, three under field conditions, revealed δ = 0.48 and 0.68, depending on how multiplicative fitness was estimated. The values were consistent with the outcrossed mating system of populations and high enough to oppose the spread of self-fertilization, unless pollinators or mates limit fertility, but lower than is frequently reported in other outcrossing plant species. In summary, this research provides novel information on the mechanisms that maintain tristyly in invasive populations of L. salicaria, despite the occurrence of partial self- incompatibility. High rates of inter-morph mating promoted by reliable bee-mediated pollinator service limit opportunities for the breakdown of the polymorphism, an evolutionary transition that has commonly occurred in other invasive tristylous species. iii ACKNOWLEDGEMENTS My PhD thesis would not have been possible without extensive help from many individuals and organizations. First, I would like to thank my PhD supervisor Spencer Barrett, whose knowledge on plant life history and reproductive biology, highly attuned writing skills, and apparently endless energy and enthusiasm for science have been absolutely necessary for my thesis completion. I have benefited immensely from his guidance in my graduate training and will not forget his contributions to my growth professionally as a scientist and personally. I also thank my committee members James Thompson and John Stinchcombe for providing invaluable feedback on my project over the last 5+ years, as well as Peter Kotanen, Helen Rodd, and Art Weis who have served on my defence committee and Stephen Wright who assisted with my appraisal. I thank my external examiner Stephen Weller for his thoughtful feedback and questions on my thesis and during my defence. Finally, I thank Andrew Stephenson and the members of the Stephenson lab for introducing me to plant mating systems and the questions which abound in them. Additionally, I thank Christopher Eckert and Robert Colautti at Queens University whose works on the invasion genetics of Lythrum salicaria were pivotal to my studies on this system. I thank the other members of the Barrett Lab including Ramesh Arunkumar, Stuart Campbell, Julia Charlebois, Joana Costa, Daisy Crowson, Nicolay Cunha, Josh Hough, Zoe Humphries, Wan Jin, Joana Rifkin, Andrew Simpson, David Timerman, Haoran Xue and Wei Zhou who have provided intellectually stimulating discussion as well as useful guidance at various time during my thesis research at the University of Toronto. I also thank members of the Department of Ecology and Evolutionary Biology iv particularly Megan Greischar, Eddie Ho, Tyler Kent, Julia Kreiner, Jason Laurich, Vanessa Nielsen, Rebecca Schalkowski, Sarah Steele, Matt Stata, Stefanie Sultmanis, Alison Wardlaw, Corlett Wood and Amanda Xerub for their advice and support. I would not have been able to gather the data required to complete my thesis without endless hours of assistance from a multitude of undergraduate assistants. I am especially grateful to Cole Brookson, Jamy Fu, Sahil Gupta, Dowon Lee, Teresa Maddison, Tobias Mankis, Baily McCollough, Fernanda Pazin, Shirley Qiu, and Carol Wong for all of their help with data collection in the field, glasshouse and laboratory. I thank Bill Cole for providing advice and logistical support in the glasshouse and in the field as well as Andrew Petrie and Bruce Hall for their assistance with horticulture and the growing of thousands of Lythrum salicaria plants in the glasshouse. I thank Stephen Schneider and John Jensen at the Koffler Scientific Reserve in providing assistance with setting up my experiments, maintenance and troubleshooting in the field. Without these individuals I would not have been able to properly conduct the large-scale field experiments that I required for making this thesis a success. The doctoral research that comprises this PhD thesis was funded by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to Spencer Barrett, as well as by student scholarships from the Department of Ecology and Evolutionary Biology, University of Toronto. Finally, I thank my parents Robert and Karla Balogh for their unwavering support during my time at the University of Toronto. I also thank my wife Jennifer Balogh for her love, patience and emotional support especially during the long stretches I was away from v Pennsylvania. I also thank her for assistance in putting the final thesis togther over the past few months. Finally, I thank coffee – coffee made everything possible. vi TABLE OF CONTENTS ABSTRACT ........................................................................................................ II ACKNOWLEDGEMENTS ......................................................................................... IV TABLE OF CONTENTS ............................................................................................VII LIST OF TABLES ........................................................................................................ X LIST OF FIGURES ..................................................................................................... XI LIST OF APPENDICES ........................................................................................... XIV CHAPTER 1 GENERAL INTRODUCTION ......................................................... 1 Invasion genetics and reproductive systems ................................................................. 1 Uniparental reproduction and colonization................................................................... 3 Tristyly and colonization ............................................................................................. 9 Colonization and inbreeding depression..................................................................... 15 Study system: Lythrum salicaria ............................................................................... 18 Thesis objectives ....................................................................................................... 22 CHAPTER 2 THE INFLUENCE OF PARTIAL SELF- INCOMPATIBILITY AND AUTOTETRAPLOIDY ON FLORAL MORPH FREQUENCIES IN FINITE TRISTYLOUS POPULATIONS .................................... 27 Abstract ..................................................................................................................... 27 Introduction ............................................................................................................... 28 Material and Methods ................................................................................................ 34 Results ...................................................................................................................... 36 Discussion ................................................................................................................. 47 CHAPTER 3 STOCHASTIC PROCESSES DURING INVASION: THE INFLUENCE OF POPULATION SIZE ON STYLE-MORPH FREQUENCY VARIATION IN LYTHRUM SALICARIA (PURPLE LOOSESTRIFE) ....................................................................................................... 60 Abstract ....................................................................................................................
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