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Pollinator Specialization and the Evolution of Pollination Syndromes in the Related Silene , S

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Pollinator Specialization and the Evolution of Pollination Syndromes in the Related Silene , S ABSTRACT Title of Document: POLLINATOR SPECIALIZATION AND THE EVOLUTION OF POLLINATION SYNDROMES IN THE RELATED SILENE , S. CAROLINIANA , S. VIRGINICA , AND S. STELLATA Richard James Reynolds, Ph.D., 2008 Directed By: Associate Professor, Charles B. Fenster, Biology Associate Professor, Michele R. Dudash, Biology Pollination syndromes are the convergent expression of floral traits in unrelated species reflecting specialized interactions between plants and pollinators exerting similar selection pressures. I addressed the controversial claim that pollinator- mediated selection is unlikely to be a major factor underlying floral evolution because plants often have many functionally different floral visitors. Detailed pollination data and pollinator-mediated selection studies are needed to address the notion that specialized plant-pollinator interactions are a major mechanism of floral evolution. I developed statistical methods to measure the importance of pollinators (Chapter 1). I addressed whether floral morphological differences of the related Silene species, S. caroliniana , S. virginica , and S. stellata , correspond to predicted specialized pollination systems (Chapter 2). I asked whether contemporary selection pressures on floral traits were detectable in a population of S. virginica (Chapter 3). I investigated the non-obligate interaction of S. stellata and the moth Hadena ectypa , that pollinates it and uses its immature seed for the development of larval offspring (Chapter 4). Using my novel methodology (Chapter 1), I demonstrated that S. virginica and S. stellata were specialized on hummingbirds and nocturnal moths, respectively (Chapter 2). S. caroliniana was least specialized with long-tongued diurnal hawkmoth ( Hemaris sp ) and large bee pollinators ( Bombus spp. and Xylocopa virginiana ). These results matched predictions based on interspecific differences in Silene floral trait expression and were consistent with the notion that the important pollinators are the major selective agents on floral design. Positive directional but mainly nonlinear hummingbird-mediated phenotypic selection (Chapter 3) on S. virginica floral traits was detected through lifetime fitness components, supporting predictions from the syndrome concept. Flowering date predicted the relative density of H. ectypa and other moth pollinators of S. stellata , and H. ectypa density varied by population and year, which may determine the sign of the H. ectypa-S. stellata interaction. Both curvature and directional selection in S. stellata ’s floral trait selection surface were context dependent on the intensity of H. ectypa larval fruit predation. Overall pollinators are important sources of selection underlying floral evolution in these Silene , and S. stellata floral evolution is subject to additional selection pressures from H. ectypa larvae. POLLINATOR SPECIALIZATION AND THE EVOLUTION OF POLLINATION SYNDROMES IN THE RELATED SILENE , S. CAROLINIANA , S. VIRGINICA , AND S. STELLATA By Richard James Reynolds Dissertation submitted to the Faculty of the Graduate School of the University of Maryland, College Park, in partial fulfillment of the requirements for the degree of Doctor of Philosophy 2008 Advisory Committee: Dr. Charles B. Fenster, Co-Chair Dr. Michele R. Dudash, Co-Chair Dr. Bahram Momen Prof. David W. Inouye Prof. William F. Fagan Prof. Gerald S. Wilkinson © Copyright by Richard James Reynolds 2008 Acknowledgements I want to thank my advisors, Charlie Fenster and Michele Dudash, for their support and encouragement throughout my doctoral training. I benefited from their mentoring. I also thank my committee members R. Denno, B. Momen, D. Inouye, W. Fagan, and J. Wilkinson for thoughtful and careful comments and corrections on my thesis. I thank the outside faculty members S. Kephart of Willamette University and M. Blows of University of Queensland. Specifically for Chapter 1, I thank A. Royer, S. Marten-Rodriguez, and K. Barry for field assistance, W. Fagan and B. Momen for discussions of the methodology, M. Larsson for discussion of the standard error of importance. I thank D. Inouye, M. Dudash, J. Hereford, M. Rutter, A. Kula, J. Silander (AE), and two anonymous reviewers for comments on the manuscript. I also thank the National Park Service and C&O Canal National Park personnel for permitting us access to field study sites. This research was sponsored by the Washington Biologists Field Club, The Nature Conservancy’s Biodiversity Conservation Research Fund, and NSF DEB-0108285 to C. Fenster and M. Dudash. Specifically for chapter 2, I thank H. Wilbur and E. Nagy for thoughtful discussions and logistical and technical assistance. I thank M. Westbrook, J. Cridland, A. Rhode, N. Mahmood and A. Royer for work in the field and laboratory, and M. Pogue of USDA’s Agricultural Research Service, Systematic Entomological Laboratory for moth identification. I thank W. Fagan D. Inouye, G. Wilkinson, B. Momen, and lab members, S. Marten-Rodriguez, and K. Barry for comments on the manuscript and/or field assistance and the National Park Service and C&O Canal National Park for permitting us ii access to study sites. This research was sponsored by the Washington Biologists Field Club, The Nature Conservancy’s Biodiversity Conservation Research Fund, and NSF DEB-0108285 to C. Fenster and M. Dudash. Specifically for Chapter 3, I thank H. Wilbur, E. Nagy, and E. Brodie for advice and support at MLBS. I also thank G. Cheely, P. Stevens, J. Westbrook, J. Ash, A. Royer, C. Williams, A. Rhode, J. Malin, for field research assistance, and J. Cridland and R. Boateng for laboratory assistance and W. Fagan, D. Inouye, B. Momen and J. Wilkinson for comments on earlier versions of this chapter. The authors thank M. Blows for discussions of multivariate selection. This research was supported by MLBS and NSF DEB-0108285 to C. Fenster and M. Dudash. Specifically for chapter 4, I thank R. Denno, W. Fagan, D. Inouye, B. Momen, and J. Wilkinson, for advice in project design and for comments on the manuscript. I also thank J. Westbrook, J. Ash, A. Rhode, C. Williams, J. Malin, A. Kula, J. Cridland and W. Dwyer for field or laboratory assistance. I thank M. Pogue for moth identification. We thank E. Nagy and H. Wilbur for logistical and technical assistance. This research was funded by NSF DEB-0108285 to C. Fenster and M. Dudash. iii Table of Contents ACKNOWLEDGEMENTS................................................................................................II TABLE OF CONTENTS.................................................................................................. IV CHAPTER 1: POINT AND INTERVAL ESTIMATION OF POLLINATOR IMPORTANCE: A STUDY USING POLLINATION DATA OF SILENE CAROLINIANA ................................................................................................................... 1 CHAPTER 2: POLLINATOR SPECIALIZATION AND POLLINATION SYNDROMES OF THREE RELATED NORTH AMERICAN SILENE ....................... 22 CHAPTER 3: MULTI-YEAR STUDY OF MULTIVARIATE LINEAR AND NONLINEAR PHENOTYPIC SELECTION ON FLORAL TRAITS OF HUMMINGBIRD-POLLINATED SILENE VIRGINICA ................................................ 65 CHAPTER 4: EVALUATING SPATIAL AND TEMPORAL VARIATION IN THE INTERACTION OF THE NURSERY POLLINATOR, HADENA ECTYPA (LEPIDOPTERA: NOCTUIDAE) AND ITS HOST, SILENE STELLATA (CARYOPHYLLACEAE): ECOLOGICAL AND EVOLUTIONARY IMPLICATIONS. ......................................................................................................................................... 126 APPENDICES ................................................................................................................ 184 BIBLIOGRAPHY........................................................................................................... 187 iv Chapter 1: Point and interval estimation of pollinator importance: A study using pollination data of Silene caroliniana . Abstract Pollinator importance, the product of visitation rate and pollinator effectiveness, is a descriptive parameter of the ecology and evolution of plant-pollinator interactions. Naturally, sources of its variation should be investigated, but the standard error of pollinator importance has never been properly reported. Here, a Monte Carlo simulation study and a result from mathematical statistics on the variance of the product of two random variables are used to estimate the mean and confidence limits of pollinator importance for three visitors of the wildflower, Silene caroliniana . Both methods provided similar estimates of mean pollinator importance and its interval if the sample size of the visitation and effectiveness datasets were comparatively large. These approaches allowed us to determine that bumblebee importance was significantly greater than clearwing hawkmoth which was significantly greater than bee fly. The methods could be used to statistically quantify temporal and spatial variation in pollinator importance of particular visitor species. The approaches may be extended for estimating the variance of more than two random variables. However, unless the distribution function of the resulting statistic is known, the simulation approach is preferable for calculating the parameter’s confidence limits. Keywords Pollinator effectiveness ⋅ Pollinator visitation ⋅ Variance of product ⋅ Floral specialization ⋅ Floral generalization 1 Introduction Beginning with Stebbins’ (1970) assertion that floral traits evolve in response to the most effective and abundant pollinators, pollination ecologists
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