Multilocus assessment of population differentiation in Baja California birds: implications for community assembly and conservation A DISSERTATION SUBMITTED TO THE FACULTY OF UNIVERSITY OF MINNESOTA BY Hernan Vazquez Miranda IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY F. Keith Barker and Robert M. Zink August 2014 © Hernan Vazquez Miranda 2014 Acknowledgements I would like to thank numerous people that made writing this dissertation possible. First and foremost I thank my advisers Keith Barker and Bob Zink. They mentored me in every way, from finding and developing my own research interests to formulating innovative ideas, effective and concise scientific writing, and learning how to obtain my own funding. They are the embodiment of human and academic kindness. My committee members, Ken Kozak and Peter Tiffin, helped me develop my ideas and expand my perspectives; they often pushed me to think “outside the bird box”. I thank members of the Systematics Discussion Group for debates on principles, methods, and insights that improved my understanding on how species originate and diversify. In particular I would like to thank my friends Ben Lowe, Matt Dufort, Tom Giarla, Liz Wallace, Lorissa Fujishin, Domink Halas, Chih-Ming Hung, Tricia Markle, Juan Diaz, and Tony Gamble for their honest and constant advice on my progress and new ideas. Numerous people and institutions provided me with tissue loans. I am grateful to the curators of the Bell Museum of Natural History-University of Minnesota (BMNH), A. Navarro-Sigüenza from the Museo de Zoología “Alfonso L. Herrera”-Universidad Nacional Autónoma de México (MZFC), J. Klicka and S. Birks from the Burke Museum of Natural History-University of Washington (UWBM), K. Burns from San Diego State University (SDSU), D. Dittmann and R. Brumfield from the Louisiana State University Museum of Natural Science (LSUMNS), N. Rice from the Academy of Natural Sciences of Philadelphia (ANSP), M. Robbins from University of Kansas (KU), P. Sweet from the American Museum of Natural History (AMNH), K. Rabenold from Purdue University, J. i Hinshaw from the University of Michigan Museum of Zoology (UMMZ), and B. Marks and D. Willard from the Field Museum of Natural History (FMNH). My collaborators in Mexico, Adolfo Navarro, Vicente Contreras, Roberto Sosa, and Octavio Rojas helped me immensely to plan and conduct my fieldwork successfully. I would also like to acknowledge Mexican authorities for making my fieldwork a smooth process. Jaime Castro and Erick Rodriguez, Avery Michenzi, Carolyn Disse, Jordan Herman, and Leah VandenBosch assisted me in multiple lab and field procedures. I received funding from multiple institutions to pay for research expenses. The University of Minnesota supported my research in multiple capacities: several Dayton- Wilkie Award from the Bell Museum of Natural History, an International Graduate Student Grant from the Graduate School, two Huempfner Fellowships, and one Anderson Fellowship. I am also grateful to the Chapman Fund of the American Museum of Natural History and a Graduate Student Grant from the American Ornithologists’ Union for funding the initial stages. The Consejo Nacional de Ciencia y Tecnología of Mexico (CONACyT) gave me a scholarship for part of my stipend during four years. Several analyses were executed on the Minnesota Super Computer Institute and the CIPRES portal (Miller et al. 2010); I thank Matthew Miller for his computer assistance. I also thank Lynx Edicions for allowing me to reproduce HBW bird illustrations. Finally I would like to thank a number of friends beyond count in Minnesota and Mexico that made my time away from home enjoyable, allowing me to finish this process. My family, and in particular my mother, gave me every kind of love and support to follow my dreams and to learn how to fly. ii Dedication I dedicate this dissertation to my mother Susana Miranda, my friends everywhere, the Land of 10,000 Lakes, and Baja California; the origin and the destination. And of course to cohorts of incredible ducklings, cubs, and kits that taught me the most important lesson in life: It’s Duck Duck Gray Duck and none of that goose nonsense. iii Abstract This dissertation is an assessment of biological diversification at the community, species, and population levels from large continental scales in the Americas to small regions between Mexico and the U.S. using birds as a study system. In Chapter 1, I calculate when the avian community of the Baja California peninsula diverged from the mainland using mitochondrial and nuclear DNA sequences. I discovered that even though birds fly and could have arrived to the peninsula in independent dispersal waves, genetic estimates correspond to few events of diversification that correspond to historical barriers to gene flow and more recent ecologic scenarios. Additionally, I find evidence for recognizing four peninsular lineages as valid species, doubling the number of endemic birds in Baja California. Chapter 2 is a collaboration with Keith Barker. In it, we explore the continental diversification of wrens in the genus Campylorhynchus solving all evolutionary relationships by sequencing 23 genes and multiple individuals per lineage, developing a new metric for comparing all sorts of phylogenetic trees, and clarifying biogeographic and behavioral evolution aspects in the Neotropics. In Chapter 3, me and collaborators Kelly Barr, Craig Farquhar, and Robert Zink merge historic fire ecology and population genetics to understand how and when the black-capped vireo (Vireo atricapilla), went from being a historically common bird to being considered currently as endangered in its breeding grounds in the oak savannas of Oklahoma, Texas and northern Mexico. Five online supplementary files (OSFs) accompany this dissertation: the first file includes voucher numbers, geographic information, substitution models, used primers, and full likelihood values in Chapter 1 (OSF 1); the second file contains Bayesian trees iv and taxon pair distributions in Chapter 1 (OSF 2); the third file includes voucher numbers, evolutionary models, recombination tests, and primers used in Chapter 2 (OSF 3); the fourth file includes the randomization design in Chapter 2 (OSF 4); and the fifth file includes geographic information for all samples, primers, and multilocus phylogeny of vireos used in Chapter 3 (OSF 5). v Table of Contents List of Tables ……………………………………………………………………………vii List of Figures …………………………………………………………………………..viii Chapter 1: Congruence despite biogeographic complexity: multilocus assessment of divergence in Baja California birds ..……………………………….….………………....1 Introduction …………………………………………………………………….....1 Materials and Methods …………………………………………………................6 Results …………………………………………………………………...............13 Discussion …………………………………………………………….................18 Chapter 2: The phylogenetic power of sex at the species level resolves evolutionary relationships among Neotropical wrens ............................................................................30 Introduction ……………………………………………………………………...30 Materials and Methods …………………………………………………..............34 Results …………………………………………………………………...............42 Discussion …………………………………………………………….................52 Chapter 3: Fluctuating fire regimes and their historical effects on genetic variation in an endangered savanna specialist ..........................................................................................68 Introduction ……………………………………………………………………...68 Materials and Methods …………………………………………………..............72 Results …………………………………………………………………...............78 Discussion …………………………………………………………….................82 Bibliography ....................................................................................................................89 Appendices .....................................................................................................................103 Appendix 1: Time calibrated species tree phylogeny of Campylorhynchus........103 vi List of Tables Table 1. Taxon pairs of Baja California birds ..................................................................28 Table 2. Summary statistics per locus in the black-capped vireo ....................................79 Table 3. Summary statistics per black-capped vireo locality ...........................................79 vii List of Figures Figure 1.1. Map of Baja California ....................................................................................4 Figure 1.2. Splitting times (in millions of years) for all taxon pairs using BEAST.........15 Figure 1.3. Prior testing and posterior probabilities for number of splitting events ........16 Figure 1.4. Coalescent-based time estimates for splits in co-distributed taxon pairs ......17 Figure 2.1. Trees from analyses of the five locus dataset ................................................63 Figure 2.2. Trees from analyses of the 23 locus dataset ..................................................64 Figure 2.3. Cloudograms of species trees ........................................................................65 Figure 2.4. Locus clade support variability and distribution of the HSN index ..............66 Figure 2.5. Locus rarefaction curves from randomizations .............................................67 Figure 3.1. Breeding sampling localities and Bayesian genotype cluster assignment......71 Figure 3.2. Likelihood values of inferred number of genetic clusters .............................80 Figure 3.3.