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Global Population Genetics and Evolution of Invasive Biotypes in the Whitefly Complex Bemisia tabaci By Margarita Hadjistylli A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Environmental Science, Policy, and Management in the Graduate Division of the University of California, Berkeley Committee in charge: Professor George K. Roderick, Chair Professor Rosemary G. Gillespie Professor Craig Moritz Fall 2010 Global Population Genetics and Evolution of Invasive Biotypes in the Whitefly Complex Bemisia tabaci © 2010 by Margarita Hadjistylli Abstract Global Population Genetics and Evolution of Invasive Biotypes in the Whitefly Complex Bemisia tabaci by Margarita Hadjistylli Doctor of Philosophy in Environmental Science, Policy, and Management University of California, Berkeley Professor George K. Roderick, Chair The presence of morphologically cryptic lineages with divergent molecular, ecological, and physiological traits within a species is an intriguing evolutionary phenomenon that offers unique opportunities for evolutionary genetics studies. One such system is the whitefly species complex Bemisia tabaci (Hemiptera: Aleyrodidae), which comprises several cryptic lineages, known as “biotypes” with worldwide distribution, including two of the world’s worst invasive pests. In this dissertation I take a population genetics approach to examine the global genetic structure of B. tabaci biotypes, with a focus on the origins, historical demography, and invasion pathways of the two invasive biotypes, known as “B” and “Q”. I begin with a historical overview of multilocus molecular markers used to examine aspects of the biology, ecology, and genetics of the B. tabaci species complex. The first markers employed were allozymes, particularly esterases, which became the basis for the biotype nomenclature, and were substantiated by ecological and biological data. The exploration of various DNA based markers has established that biotypes within B. tabaci are exceptionally diverse genetically, in spite of their identical morphologies. Global population genetics analyses using microsatellite markers showed that well- characterized B. tabaci biotypes correspond to real genetic entities with strong geographic structure, and limited or no gene flow among them. The resulting genetic clusters from this analysis are in general agreement with the only well-resolved global phylogeny of the species, which is based on a single mitochondrial gene (cytochrome oxidase I). However, some cases of conflict in the two sets of markers do exist, perhaps associated with the different modes of inheritance, thus cautioning against the use of mitochondrial DNA as a single marker for species or subspecies delineation. Analysis of genetic data with more sophisticated Bayesian coalescent-based approaches offers the opportunity to study both contemporary and ancestral invasion pathways. Using such an approach, I showed that divergence histories of the invasive biotypes B and Q coincided with periods of extensive human movement and trade of agricultural 1 goods in the Mediterranean, the Middle East, and Africa during the Iron and Bronze Ages, and the Roman period. Results also indicate that ancestral populations to the current B and Q biotypes had much larger effective sizes than those of emerging biotypes, a pattern consistent with expectations of diversification in invasive species. In a contemporary context, I investigated the recent invasion history of biotype Q in the USA. I found that populations introduced into the USA originated from both the Western and Eastern Mediterranean, in at least three independent cryptic invasions, and spread directly from a single initial introduction site, likely through plant trade. Findings from this dissertation underscore the practical importance of better monitoring invasions of this insect and other invasive pests at points of entry and dispersal through trade of plant material. From a theoretical perspective, this work adds insights into the origins of biotypes, both in the B. tabaci complex and more generally, emphasizing the demographic processes involved in diversification of invasive biotypes. The research highlights the potential to use B. tabaci in studies of broader applied as well as evolutionary significance. 2 Dedication To my parents for all the sacrifices they made for my education and to my husband, Menelaos, for standing by me throughout the whole journey i Table of contents Acknowledgements iv Introduction 1 Chapter 1: Review of molecular markers used in population genetics studies of Bemisia tabaci Abstract 8 Introduction 9 Protein markers 10 DNA-level markers 15 DNA-level PCR-based markers 17 Additional considerations and future directions 30 Conclusions 32 References 34 Tables 43 Chapter 2: Global population genetics of a worldwide pest: genetic diversity and population structure in the Bemisia tabaci cryptic species complex Abstract 47 Introduction 48 Materials and Methods 50 Results 54 Discussion 57 References 64 Tables 70 Figures 75 Chapter 3: Historical demography and divergence of the invasive Bemisia tabaci biotypes B and Q associated with human movement and trade in the Mediterranean, Middle East, and Africa Abstract 83 Introduction 84 Materials and Methods 85 Results 88 Discussion 89 References 93 Tables 97 Figures 100 ii Chapter 4: Evidence for multiple independent and cryptic invasions of the whitefly Bemisia tabaci biotype Q in the USA Abstract 106 Introduction 107 Materials and Methods 109 Results 113 Discussion 117 References 122 Tables 127 Figures 133 Conclusions 144 iii Acknowledgements I would like to begin by thanking George Roderick, my advisor and Chair of my Dissertation Committee. George was supportive of any initiative I pursued for my research and motivated me to keep up with my goals, while making sure that financial issues were the last thing to worry about during my studies. His encouragement for my participation in conferences and meetings worldwide helped me make connections and opened my mind to the academic world. I feel fortunate to have worked with George on an exciting research project and because through his mentoring I learned how to approach scientific questions and research in general. I am greatly indebted to my Dissertation Committee members, Rosemary Gillespie and Craig Moritz, who gave me constructive comments and feedback from the beginning of my project to the final drafts of my dissertation. The opportunity to teach with, and be taught from Craig has been one of my most rewarding experiences at Berkeley, and inspired my interest in biology and evolution. I am also very grateful to Steve Welter and Vince Resh who have been great teachers and because our interactions helped shape my thinking as a researcher and teacher. My research would not have been possible without Judith Brown of the University of Arizona, Tucson. As a professor with renowned whitefly expertise, she gave me constant feedback throughout my studies. In addition, Judith provided me with whitefly samples from her collection and gave me access to her lab, where I received my first molecular training from Donald Rogan. Furthermore, she helped me make connections with whitefly researchers from around the world. I am also indebted to many colleagues worldwide for contributing whitefly specimens, especially P. Bleeker, D. Bosco, C. Erdogan, P. De Barro, H. Delatte, N. Gauthier, K. Goodman, E. Hernandez, R. Horowitz, J. Imamura, and L. Papayiannis. I would also like to acknowledge the funding I received from various sources: UC Berkeley, Department of Environmental Science, Policy and Management, Division of Organisms and Environment, Berkeley International Office, USDA-NRI, France- Berkeley Fund, NSF RCN: Invasive Insects, Moorea Biocode Project, Margaret C. Walker Fund Award for Systematic Entomology, William Carroll Smith Fellowship, Julius Freitag Memorial Award, and Robert L. Usinger Memorial Fund. I especially acknowledge the three-year educational grant from the A.G. Leventis Foundation in Cyprus. I would also like to thank the Ministry of Agriculture and the Government of Cyprus for the educational leave provided to me for doctoral studies. At Berkeley, I would like to thank my labmates in the “Evolab” who have been great friends, and gave me wonderful moments to remember, from the lab bench, to the field, and to our nights out. I especially thank Pete Croucher whose guidance and help with genetic data analysis has been enormous; from him I learned how to be conscientious in research. I also thank Sean Schoville and Jeff Lozier for their help with molecular lab work. I feel very lucky that I had the opportunity to work with talented undergraduate students, especially Theresa Canavan, Jeff Sorokin, and Danielle Jones. Most of all however, I am grateful to have worked with Athena Lam, who helped me become a better teacher by being an ideal student. Her contribution to my research improved it significantly and her presence made my long hours in the lab more enjoyable. iv Kari Roesch Goodman has been a key figure from the beginning to the end of my PhD studies and I feel fortunate to have gone through orals, teaching, conferences, lab work and data analysis with a friend close to me. Our dissertation group meetings, along with Pauline Kamath and Emily Rubidge helped me enormously – but above all I am thankful for our friendship. Natalia Choussou-Polydouri, Diamantis Sellis, Pete Oboyski, Jennifer Imamura, and Sal, have been great friends inside

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