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The Ecology and Genetics of Adaptation and Speciation in Dune

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The Ecology and Genetics of Adaptation and Speciation in Dune THE ECOLOGY AND GENETICS OF ADAPTATION AND SPECIATION IN DUNE SUNFLOWERS by Katherine Lee Ostevik H.B.Sc., The University of Toronto, 2008 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Botany) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) March 2016 © Katherine Lee Ostevik, 2016 Abstract We can learn about the factors that promote and constrain speciation by comparing multiple instances of the evolution of reproductive isolation. It is particularly useful to compare systems with similar environmental transitions because natural selection is likely responsible for any evolutionary patterns that are consistently associated with ecological variation. In this thesis, I examine two cases of putatively similar recent or incipient ecological speciation in the sunflower genus Helianthus. In each case, the divergence observed between geographically adjacent populations is associated with adaptation to sand dunes. In my first study, I comprehensively test for reproductive isolation between dune and non-dune ecotypes of H. petiolaris. Despite their recent divergence, I find that multiple reproductive barriers separate them, including post- pollination assortative mating in the form of pollen competition. In addition, I find that a striking difference in seed size between the ecotypes is a consequence of divergent natural selection, and that it leads to strong and extrinsic reproductive isolation via selection against immigrants and hybrids. I then broaden my study to include the dune endemic, H. neglectus, which is sister to typical H. petiolaris. I look for chromosomal rearrangements between H. neglectus and H. petiolaris, and find almost as many large translocations between them as between more distantly related sunflowers. Finally, I discover that larger seeds are associated with dune environments in both systems and that the genetic basis of that phenotypic evolution is partiality repeated. Taken together, these results suggest that dune adaption within H. petiolaris and between H. petiolaris and H. neglectus has similar consequences. However, it remains to be seen whether assortative mating and chromosomal evolution are unique to the evolution of dune H. ii petiolaris and H. neglectus, respectively. Ultimately, understanding the similarities and differences between these systems will help answer the question - how predictable is speciation? iii Preface I was the primary force behind the design, execution, analysis and presentation of this research. Nevertheless, several others made meaningful contributions to the final product. My advisors, Loren Rieseberg and Sarah Otto, gave me intellectual guidance in the form of advice and feedback throughout, and several research assistants and technicians helped me cultivate and cross sunflowers, collect data in the field and greenhouse, and do basic lab work. Other exceptions are listed below: Rose Andrew designed and carried out the test of hybrid fertility (chapter 2) and generated the backcrossed seeds (chapter 2), Matt Barbaur separated bees from wasps for pollinator identification (chapter 2), the USDA ARS Bee Biology & Systematics Laboratory identified bee species (chapter 2), Greg Baute made the crosses used for linkage analysis (chapter 3), Chris Grassa cultivated H. annuus x H. petiolaris seedlings (chapter 3) and Nadia Chaidir extracted H. annuus x H. petiolaris DNA (chapter 3). I am preparing manuscripts that describe the work is chapters 3 and 4, and a version of chapter 2 has been submitted for publication: Ostevik, KL, RL Andrew, SP Otto and LH Rieseberg. Multiple reproductive barriers separate recently diverged sunflower ecotypes. Also, some of the ideas and paragraphs in chapter 1 are published in: Ostevik, KL, BT Moyers, GL Owens and LH Rieseberg. 2012. Parallel ecological speciation in plants? International Journal of Ecology 2012. iv Table of Contents Abstract ......................................................................................................................................... ii Preface .......................................................................................................................................... iv Table of Contents .........................................................................................................................v List of Tables ............................................................................................................................... ix List of Figures ............................................................................................................................... x List of Abbreviations ................................................................................................................ xii Acknowledgements ................................................................................................................. xiii Dedication ................................................................................................................................. xiv Chapter 1: Introduction ...............................................................................................................1 1.1 Background ...................................................................................................................... 1 1.2 This thesis ......................................................................................................................... 3 1.2.1 Study system ............................................................................................................... 4 1.2.2 Breakdown of chapters ............................................................................................. 10 Chapter 2: Multiple reproductive barriers separate recently diverged sunflower ecotypes 14 2.1 Introduction ................................................................................................................... 14 2.2 Methods............................................................................................................................ 16 2.2.1 Study system and seed collections ............................................................................ 16 2.2.2 Calculating barrier strength ....................................................................................... 18 2.2.3 Reciprocal transplant ................................................................................................ 20 2.2.4 Timelapse photography of flowering ........................................................................ 24 2.2.5 Insect visitation and collections ................................................................................ 25 v 2.2.6 Pollen competition, seed set and pollination timing experiments ............................. 27 2.2.7 Hybrid seed germination ........................................................................................... 29 2.2.8 Pollen staining ........................................................................................................... 30 2.3 Results .............................................................................................................................. 31 2.3.1 Reproductive barrier strengths .................................................................................. 31 2.3.2 Selection against immigrants .................................................................................... 34 2.3.3 Flowering time .......................................................................................................... 38 2.3.4 Pollinator assemblage ............................................................................................... 40 2.3.5 Post-pollination assortative mating ........................................................................... 42 2.3.6 Intrinsic hybrid inviability ........................................................................................ 43 2.3.7 Hybrid pollen sterility ............................................................................................... 44 2.3.8 Selection against hybrids .......................................................................................... 45 2.3.9 Total reproductive isolation ...................................................................................... 46 2.4 Discussion ........................................................................................................................ 46 2.5 Conclusion ....................................................................................................................... 51 Chapter 3: Rapid chromosomal evolution between closely related sunflower species ..........52 3.1 Introduction ................................................................................................................... 52 3.2 Methods............................................................................................................................ 55 3.2.1 Study species and crosses ......................................................................................... 55 3.2.2 Genotyping ................................................................................................................ 56 3.2.3 Genetic mapping ....................................................................................................... 57 3.2.4 Synteny Analysis ...................................................................................................... 57 3.3 Results
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