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Rapid Evolution in Wild Radish (Raphanus Raphanistrum, L

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Rapid Evolution in Wild Radish (Raphanus Raphanistrum, L RAPID EVOLUTION IN A CROP-WEED COMPLEX (RAPHANUS SPP.) DISSERTATION Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Lesley Geills Campbell, M. S. * * * * * The Ohio State University 2007 Dissertation Committee: Approved by: Professor Allison Snow, Adviser Professor Lisle Gibbs _________________________________ Professor Maria Miriti Adviser Evolution, Ecology, and Organismal Biology Graduate Program ABSTRACT The development and adoption of transgenic crops with novel traits has raised awareness of the potential for weed populations to evolve increased weediness after hybridization with cultivated relatives. I explored the evolutionary and ecological consequences of gene flow between crop radish (Raphanus sativus) and its weedy relative (wild radish, R. raphanistrum). Hybridization may generate the genetic and phenotypic variation necessary for an evolutionary response by weeds. First, I imposed artificial selection on wild and hybrid lineages for four generations for early flowering a potentially advantageous trait for weeds. Hybrid lineages evolved more rapidly under selection for early flowering and rapidly recovered a wild-type phenology and fertility. Second, I established replicated wild and hybrid populations in agricultural landscape and measured their evolutionary response to natural conditions after three generations. Natural conditions favoured larger plants in both wild and hybrid populations. However, because an advantageous trait, large size, had been transferred to hybrid populations, hybridization resulted in significantly larger hybrid than wild weeds and accelerated weed evolution. Further, I asked whether environmental context affected the success of hybrid relative to wild radish. Using a response surface competition experiment, I examined the consequences of competition on life history and lifetime fecundity of hybrid and wild ii plants. Hybrid plants were less competitive than wild plants. With increasingly competitive conditions, differences in hybrid and wild life history and fecundity were reduced. Therefore, competition may promote the introgression of crop alleles into weed populations. In a second experiment, I examined the consequences of geographic location on fecundity of hybrid and wild plants by conducting two common garden experiments in disparate locations within the geographic range of wild radish (Michigan, California). In Michigan, hybrids had lower fecundity than wild plants, but, in California, hybrids had significantly greater fecundity and survival than wild plants, suggesting hybrids may displace wild relatives in some environments. In summary, I present new evidence for a role of hybridization in the evolution of agricultural weeds by measuring the rate of hybrid evolution relative to wild ancestors and exploring the environmental contexts that facilitate crop trait introgression into weed populations. iii DEDICATION For the patience of my mothers – Gladys, Phoebe, Claudette, Ellie, Pauline, Barb, Ellen, and Jay – and the eagerness of my Dad. iv ACKNOWLEDGMENTS My heartfelt thanks goes to Allison Snow for her encouragement, enthusiasm, and guidance during the past five years. I am also extremely fortunate to have worked with Julie Ketner, Maria Miriti, Caroline Ridley, and Patty Sweeney as collaborators. Committee members Lisle Gibbs, Libby Marschall, and Maria Miriti contributed immensely by reading proposals, critiquing papers, and, most importantly, by providing support and food for thought. The members of the Snow lab, Mike Reagon, Su Su, Patty Sweeney, Yifru Teklu, Yan Jin, Jill Johnson, Kristin Mercer, Sarena Selbo, and Lawrence Spencer, as well as the graduate associates of EEOB had a profound impact on my work through important discussions in forming many of the ideas I present and constructive criticisms of the work in early and late stages. I also very much appreciate the careful eye of Don Campbell who read and commented on each chapter. My sincere thanks also goes to the undergraduate researchers who worked so diligently with me on these projects: Karen Alofs, Anna Babayan, Marie Burleson, Sarah Clark, Nora Curiel, Alex DeCamp, Holly Eisel, Erin Hill, Scott Gifford, Julie Ketner, Nicholas Marsh, Nana Masuda, Kate Mollohan, Sarah Pfingsten, Retika Rajbhandari, Soja Sekharan, Missy Schneider, Danielle Smith, Nicole Smith, Karl Toth, Kaushik Vedam, Jenny Waterbury, David Yang. The Bonnett, Brubacher, Dotski, Gregory, Ginop, Hartman, Jarman, Jurek, Phelps, Reimann, Romanik, Schreier, Stempky, and Sterzik v families generously shared their farmland, time, and local knowledge. The University of Michigan Biological Station community (especially Knute Nadelhoffer, Kari Slavik, Lisa Readmond, Richard Spray, Tony Sutterly, Bob Vandekopple, Chris Vogel, and Ken Willoughby) and Cathy Drake, Rene Madsen, and Joan Leonard of the Ohio State University played fundamental roles in the success of these projects. Stauf’s coffeehouse, Soul Sista’s and the Huntsville Public Library provided comfortable and welcoming writing spaces. The work presented here was financially supported by the US Department of Agriculture, a National Science Foundation Doctoral Dissertation Improvement Grant, Janice Carson Beatley Herbarium Fund, University of Michigan Biological Station, The Nature Conservancy, The Ohio State University Mary S. Muellhaupt Presidential fellowship, Sigma Xi, and the Henry Gleason Fellowship. Finally, a special thanks goes to my family – Tom, Phoebe, and Dad. Without your emotional and, at times, physical support, I could not have realized this goal. Thank you for the freedom to pursue my own path - such a rare luxury in this world. Thank you, thank you, thank you. vi VITA April 7, 1975 Born – Hamilton, Ontario, Canada 1998 B.S. Plant Biology, University of Guelph, Canada 1998 – 2001 Graduate Teaching and Research Associate, University of Guelph, Canada 2001 M.S. Botany, University of Guelph, Canada 2001 – 2005 Graduate Teaching and Research Associate, The Ohio State University, USA 2006 – present Mary S. Muellhaupt Presidential Fellow, The Ohio State University, USA August 11, 2006 Married (Thomas A. Waite) – Columbus, Ohio, USA PUBLICATIONS Research Publications 1. Husband, B. C., and L. G. Campbell. 2004. Population genetic and demographic responses to novel environments: implications for ex situ plant conservation. In Ex Situ Plant Conservation Symposium: Strategies for Survival. Eds E Guerrant Jr, K. Havens, M. Maunder. Island Press. Pp. 231 - 266. 2. Snow, A. A., and L. G. Campbell. 2005. Can feral radishes become weeds? In Crop Ferality and Volunteerism. Ed. J. Gressel. CRC Press. Pp. 193-208. 3. Campbell, L. G., and B. C. Husband. 2005. Impact of clonal growth on effective population size in Hymenoxys herbacea (Asteraceae). Heredity 94 (5): 526-532. 4. Campbell, L. G., A. A. Snow, and C. E. Ridley. 2006. Weed evolution after crop gene introgression: greater survival and fecundity of hybrids in a new environment. Ecology Letters 11 (9): 1198-1209. 5. Waite, T. A., and L.G. Campbell. 2006. Controlling the false discovery rate in molecular ecology: an alternative to Bonferroni. Ecoscience 13(4): 439-442. 6. Campbell, L. G., and A. A. Snow. 2006. Competition alters life history and increases the relative fecundity of crop-wild radish hybrids (Raphanus spp.). New Phytologist doi: 10.1111/j.1469-8137.2006.01941.x FIELDS OF STUDY Major Field: Evolution, Ecology, and Organismal Biology vii TABLE OF CONTENTS Page ABSTRACT………………………………………………………………………………ii DEDICATION……………………………………………………………………………iv ACKNOWLEDGEMENTS……………………………………………………………….v VITA……………………………………………………………………………………..vii LIST OF TABLES………………………………………………………………….…..…x LIST OF FIGURES……………………………………………………………………...xv Chapters: 1. Introduction.……………………………………………………….……………..1 1.1 Ecological implications of hybridization – GEOs as one applied example…2 1.2 Raphanus as a model for the analysis of the consequences of gene flow…...3 1.3 Emerging experimental methods………………………...………………….6 1.4 Objectives……...……………………………………………………………7 2. Rapid evolution of phenology increases the fertility of crop-wild hybrids..…..9 2.1 Abstract..…………………………………………………………………….9 2.2 Introduction………………………………………………………………...10 2.3 Materials and Methods..………….………………………………………...13 2.4 Results………………………………………………………………..…….17 2.5 Discussion..…………………………………………………………..…….18 2.6 Acknowledgements………………………………………………………...22 2.7 Tables………………………………………………………………………24 2.8 Figures……………………………………………………………………...25 3. When divergent life histories hybridize: insights into weed evolution………29 3.1 Abstract…………………………………………………………………….29 3.2 Introduction………………………………………………………………...30 3.3 Materials and Methods...…………………………………………………...33 3.4 Results……………………………………………………………………...42 3.5 Discussion…………………………………………………………………..47 3.6 Acknowledgements………………………………………………………....55 3.7 Tables……………………………………………………………………….57 3.8 Figures……………………………………………………………….……..63 viii 4. Competition alters life history and increases the relative fecundity of crop- wild hybrids (Raphanus spp.)……..…………………………………………...71 4.1 Abstract……………………………………………………………………71 4.2 Introduction.………………………………………………..…………..….72 4.3 Methods ……………………………………………………………………76 4.4 Results……………………………………………………………………...86 4.5 Discussion …………………………………………………………………90 4.6 Acknowledgements………………………………………………………...94 4.7 Tables………………………………………………………………………95 4.8 Figures……………………………………………………………………106 5. Weed evolution after crop gene introgression: greater survival and
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