Spatial and Temporal Patterns of Diversification in Leaf-Toed Geckos (Phyllodactylidae: Phyllodactylus) Throughout the Mexican Dry Forest
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Spatial and Temporal Patterns of Diversification in Leaf- toed Geckos (Phyllodactylidae: Phyllodactylus) throughout the Mexican Dry Forest by Christopher Blair 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 Blair 2012 Spatial and Temporal Patterns of Diversification in Leaf-toed Geckos (Phyllodactylidae: Phyllodactylus) throughout the Mexican Dry Forest Christopher Blair Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto 2012 Abstract Understanding the ecological and evolutionary processes responsible for shaping patterns of genetic variation in natural populations is a long-standing goal in molecular ecology. Although an extensive number of recent studies focus on patterns and processes throughout tropical rain forest ecosystems, substantially less effort has been placed on tropical dry forests (TDFs); a habitat known to harbour a large percentage of Earth’s diversity. In this thesis I use leaf-toed geckos of the genus Phyllodactylus to understand both the historical and contemporary processes influencing diversification throughout Mexico’s TDFs. In Chapter 2 I isolate and characterize microsatellite markers for the gecko P. tuberculosus. Chapter 3 uses these loci to conduct a landscape genetic analysis of the species near Alamos, Sonora. I find that the inclusion of landscape variables explains more genetic variance versus Euclidean distance alone. Chapter 4 examines the evolutionary history of the P. tuberculosus group throughout western Mexico. Results suggest that habitat and climate shifts during the Miocene and Pleistocene were important divers of diversification. Chapter 5 uses microsatellite and mtDNA markers to compare historical and contemporary demographic ii parameters in P. tuberculosus. I find evidence for low historical gene flow and high female philopatry, recent reductions in population sizes, and higher correlations between landscape and contemporary gene flow versus historical gene flow and mtDNA divergence. In Chapter 6 I examine the biogeographic and taxonomic consequences of the dynamic history of Baja California. My phylogenetic results provide evidence for a trans-peninsular seaway in the Isthmus of La Paz region and suggests that P. xanti nocticolus warrants species status. My results also suggest the possibility of a seaway near the Loreto area that needs to be evaluated further. By combining multiple molecular marker-types and analytical methods, this thesis adds to our understanding of diversification processes throughout the threatened Mexican TDF. iii Acknowledgments Taking on a graduate degree, especially a Ph.D. in a foreign country with limiting funding opportunities is no easy task. Throughout our graduate programs we must learn to troubleshoot potential research issues and partition the limited time we have in an effective manner. To this end, I feel that graduate school adds a second dimension of education beyond a researcher’s focus on a specific discipline. With that said, I would first like to thank my supervisor, Prof. Bob Murphy, for all his advice and guidance over the years. Bob accepted me into his lab knowing that I did not have my own research funding, in part, because I was an international student. However, he welcomed me into his lab with open arms and gave me the freedom to pursue my own research interests and was always available for advice if needed. I also thank the remainder of my thesis committee, Prof. Allan Baker and Prof. Marie-Josée-Fortin for their insightful discussions regarding methods of statistical analysis. Special thanks also go to my fellow lab-mates Christina Davy, Andre Ngo, and Pedro Bernardo for all the help and advice they have given me. Graduate school, like life, is a continuous learning process and these individuals taught me much more than I ever thought possible. I would also like to thank graduate students from other labs at the Royal Ontario Museum (ROM) and the University of Toronto for their thoughtful discussions about research methods and philosophy. In particular, I thank Ida Conflitti, Patrick Schaefer, Ruben Cordero, Julio Rivera, Damon Dewsbury, Santiago Sanchez, Yessica Rico, Pasan Samarasin, Ilona Naujokaitis-Lewis, Oliver Haddrath, and Erika Tavares for all their help over the years. As those of us in the field know, molecular genetic laboratory work can be a stressful, time-consuming process that results in many days without the generation of data. However, throughout my time at the ROM I was fortunate to have the help from a variety of talented individuals including Amy Lathrop, Kristen Choffe, and Oliver Haddrath. These knowledgeable researchers were always close-by to lend a helping hand when needed. I also thank Christopher Law and Pedro Bernardo for all their help in the laboratory and Christopher Wilson and Christopher Kyle for their assistance with 454 sequencing. iv During my time as a Ph.D. student at the University of Toronto I had the opportunity to travel for my research. Because of Bob, I was fortunate to have the chance to conduct research on geckos throughout western Mexico. Conducting field work throughout the country over the course of three years enabled me to form new collaborations that I hope will last a lifetime. Working in Mexico also allowed me to grow as an individual and understand the lives and cultures of people from different backgrounds. I first thank my collaborator and friend Fausto Méndez de la Cruz for all of his help with logistics in Mexico including securing permits. Without Fausto, this thesis would not have been possible. Special thanks also go to his students Victor Jiménez-Arcos and Anibal Diaz de la Vega for all their help. Not only are these guys excellent herpers, but they are very knowledgeable about Mexico’s diverse ecosystems and about where and when to sample. I also thank Stephanie Meyer and Martin Gabriel Figueroa Martinez for their help with all of the Alamos work. Finally, I wish to thank Marie-Josée-Fortin and Helene Wagner for the opportunity to attend the landscape genetics conference in Santa Barbara. This was a tremendous opportunity and I hope to continue to collaborate on projects with the people I met. As research is not possible without adequate funding, I must thank the appropriate funding sources for this research. The majority of this research was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) grant (A3148) issued to Bob. Funding for lab work was also provided by the Schad Foundation at the ROM. Field work in Mexico was partly funded through a Theodore Roosevelt Memorial Grant issued by the American Museum of Natural History. Finally, and most importantly, I would like to thank my parents, Burt and Debbie Blair, and my brother, Michael Blair, for all their support over the years. Words cannot express how supportive they have been to me during my time as a struggling student. Throughout my time as a college student (over 12 years) my parents gave me the freedom to pursue my interests in life even at times when it was difficult financially. For this I will always be in your debt. Pursuing advanced degrees also takes us away from the people we care about, and although this is difficult on families, my parents understood that life is short and we must follow our hearts. You raised me to be a polite, caring, hard-working man and I always wanted to make you proud of me. I hope this thesis and degree adds to that endeavor. v Table of Contents Abstract……………………………………………………………………………………….ii Acknowledgments…………………………………………………………………………....iv Table of Contents…………………………………………………………………………….vi List of Tables……………………………………………………………………………….xiv List of Figures………………………………………………………………………..……xviii List of Appendices……………………………………………………………………..….xxiii CHAPTER 1—INTRODUCTION..........................................................................................1 1. Background………………………………………………………………………..1 2. Tropical Dry Forest……………………………………………………………….5 3. Leaf-toed Geckos………………………………………………………………….6 4. Objectives of Thesis…………………………………………………………….....7 References............................................................................................................................9 Figure Legends...................................................................................................................15 Figures................................................................................................................................16 CHAPTER 2—USING NEXT-GENERATION DNA SEQUENCING FOR RAPID MICROSATELLITE DISCOVERY IN MEXICAN LEAF-TOED GECKOS (PHYLLODACTYLUS TUBERCULOSUS)....................................................................................17 vi Abstract..............................................................................................................................17 Note...................................................................................................................................18 Acknowledgments.............................................................................................................20 References..........................................................................................................................22 Tables.................................................................................................................................24 CHAPTER 3—LANDSCAPE GENETICS OF LEAF-TOED