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The Drivers of Mitochondrial DNA Divergences

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The Drivers of Mitochondrial DNA Divergences The Drivers of Mitochondrial DNA Divergences by Pedro Henrique Bernardo 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 Pedro Henrique Bernardo, 2018 The Drivers of Mitochondrial DNA Divergences Pedro Henrique Bernardo Doctor of Philosophy Department of Ecology and Evolutionary Biology University of Toronto 2018 Abstract Mitochondrial phylogeography uses the relationship between matrilineal genealogy and geography to explain speciation, phylogeny and population structure. Several hypotheses on what maintains the parapatric matrilines have been proposed: philopatry, incomplete lineage sorting, vicariance and natural selection on female-linked traits. The small lizard Urosaurus nigricaudus of the peninsula of Baja California, Mexico and southern California, USA has six parapatric matrilines that differ by substantial mtDNA divergence. In this study, I investigate what drives and maintains the deep mtDNA discontinuities in this species. I precisely locate the mtDNA lineage breaks and investigate the presence of physical barriers in those areas. I sequence the entire mtDNA genome and then test the following hypotheses: unrestricted nDNA gene flow occurs across the species; mtDNA divergences correspond to the geological events; and that functional diversifying selection is involved in the maintenance of mtDNA discordances. I use thousands of nDNA SNP loci to test the first and last hypotheses. The time-calibrated genealogy cannot reject the ii hypothesis that the mtDNA discordances originated due to a series of vicariant events that happened on the peninsula starting in the late Miocene. For millions of years, females have dispersed beyond their place of birth, and yet, they do not cross the mtDNA contact zones. Thus, I reject the hypothesis of female philopatry as an explanation for the mtDNA discontinuities. In the mtDNA contact zones, females from two lineages co-exist in a small area with no barriers forbidding dispersal beyond the mtDNA breaks. The analysis with nDNA SNPs fails to reject the hypothesis of unrestricted nDNA gene flow throughout the peninsula (K=1). Thus, analyses also reject the hypotheses of vicariance and incomplete lineage sorting as explaining the continuing mtDNA discontinuities. Selective pressure analyses point to purifying selection as the evolutionary force acting in the mitogenome of this lizard, thus rejecting the hypothesis that habitat adaptation maintains the mtDNA discontinuities. My results reject most of the proposed hypothesis for the maintenance of mtDNA discontinuities and create exciting opportunities for further investigation on the role of other female-linked traits in the maintenance of mtDNA discontinuities, such as mito-nuclear functional compensation and female behavior. iii Acknowledgments I believe that no meaningful and pivotal transition in life, comes easily. My move to Canada from Brazil in 2010 was one of the most significant undertakings of my life. Learning a new language and adjusting to a new culture and all its nuances, has been quite an endeavor. What has made this entire mission worthwhile is the reason for my move and the most reliable and solid foundation I could have ever asked for: my precious wife, Aya Refaeli-Bernardo. I thank Aya for always standing by my side during the difficult times and for her continuous support during my Ph.D. degree. I thank my parents Maria da Graça and Jorge, my brothers João Paulo and Luiz Fernando, and Aya’s family, for their continued support and understanding during graduate school. I would like to thank my Canadian father and Ph.D. Supervisor, Prof. Robert W. Murphy. Bob has received me with open arms to his lab when I arrived in Canada, and I thank him for his guidance, financial support, friendship and for continually challenging me to become better. I also thank Bob for understanding the challenges I faced during graduate school, for supporting my new career as a Police Officer, and for allowing me to conclude my Ph.D. degree. I thank professors Deborah McLennan and Marie-Joseé Fortin who were members of my committee, for their continuous support and advice that significantly improved this thesis. I further thank professors Nathan Lovejoy, Doug Currie, Sebastian Kvist, Helen Rodd and Fernando Marques who kindly accepted the invitation to participate in my appraisal and final examinations. iv A special thanks to the lab technicians Amy Lathrop and Kristen Choffe; my fellow lab- mates Christina Davy, Christopher Blair, Kevin Kong, Santiago Sánchez-Pacheco, Santiago Sánchez-Ramírez, Mateus Pepinelli and Hollis Dahn. Tulio Soares and Olivera Joksimovic volunteered to assist with my lab work. They all contributed immensely to my project and made the lab a pleasant and fun place to work. To my Mexican colleagues Prof. Sergio Ticul Álvarez-Castañeda, Prof. Fausto Roberto Mendez-de-la-Cruz, Dr. Eduardo Felipe Aguilera-Miller, Carmen Izmene Gutiérrez-Rojas (Mene), Cintya Segura-Trujillo and Griselda Gallegos-Simental, thank you for the invaluable help in acquiring the material necessary for this thesis. I am also thankful to Dr. Yessica Rico, Jonathan R. Galina-Mehlman and Dr. Taylor Edwards for the valuable assistance during the ddRAD-seq process. I am grateful to the Royal Ontario Museum and the Department of Ecology and Evolutionary Biology at the University of Toronto (EEB) for providing an intelligent and stimulating environment during my years as a Ph.D. student. I thank York Regional Police Chief Eric Jolliffe and all my supervisors for authorizing my leave of absence to complete this thesis. A special thanks to my YRP friends Paulo Ferreira, Brad Weick and Alvaro Almeida for the continuous support and for inspiring me as examples of excellence. During my Ph.D. I was supported by a Canada Graduate Scholarship from the National Science and Engineering Research Council of Canada (NSERC), and a number of EEB grants. My research was funded through a NSERC Discovery Grant to Prof. Robert W. Murphy and field equipment was generously donated by IdeaWild. v Table of Contents Acknowledgments ............................................................................................................ iv List of Tables .................................................................................................................... xi List of Figures ................................................................................................................ xiv Chapter 1 General Introduction ................................................................................... 1 1.1 Mitochondrial DNA Discontinuities and Research Objectives .......................... 1 1.2 The Peninsula of Baja California ....................................................................... 2 1.3 Model Organism ................................................................................................. 3 1.4 Research Outline ................................................................................................ 4 1.4.1 Chapter 2: Using Maternal Ancestry Monophyly Analysis (MAMA) in the field to detect contact zones between parapatric populations .................................... 6 1.4.2 Chapter 3. The complete mitochondrial genome of the black-tailed brush lizard Urosaurus nigricaudus (Reptilia, Squamata, Phrynosomatidae) ..................... 6 1.4.3 Chapter 4. When mitochondrial phylogeography fails: female genealogy is only part of the story .................................................................................................. 7 1.4.4 Chapter 5. The drivers of deep mitochondrial DNA divergence of black- tailed brush lizard (Urosaurus nigricaudus) .............................................................. 8 Chapter 2 Using Maternal Ancestry Monophyly Analysis (MAMA) in the field to detect contact zones between parapatric populations ................................................. 10 Abstract ........................................................................................................................ 11 vi 2.1 Introduction ..................................................................................................... 12 2.2 Material and Methods ...................................................................................... 13 2.2.1 Sampling ....................................................................................................... 13 2.2.2 DNA Extraction, Amplification and Sequencing ......................................... 14 2.2.3 Development of Lineage-Specific Primers .................................................. 16 2.3 Results and Discussion ..................................................................................... 17 2.4 Figures ............................................................................................................. 20 2.5 Tables ............................................................................................................... 25 Chapter 3 The complete mitochondrial genome of the black-tailed brush lizard Urosaurus nigricaudus (Reptilia, Squamata, Phrynosomatidae). .............................. 28 Abstract ........................................................................................................................ 29 3.1 Main text ........................................................................................................... 30 3.2 Figures ............................................................................................................
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