Scale and ecological and historical determinants of a species’ geographic range: The plant parasite Phoradendron californicum Nutt. (Viscaceae) By Andrés Lira Noriega Submitted to the graduate degree program in Ecology and Evolutionary Biology and the Graduate Faculty of the University of Kansas in partial fulfillment of the requirements for the degree of Doctor of Philosophy. ________________________________ Chairperson Jorge Soberón ________________________________ Chairperson A. Townsend Peterson ________________________________ Mark E. Mort ________________________________ Craig E. Martin ________________________________ Stephen L. Egbert Date Defended: April 8, 2014 The Dissertation Committee for Andrés Lira Noriega certifies that this is the approved version of the following dissertation: Scale and ecological and historical determinants of a species’ geographic range: The plant parasite Phoradendron californicum Nutt. (Viscaceae) ________________________________ Chairperson Jorge Soberón ________________________________ Chairperson A. Townsend Peterson Date approved: April 8, 2014 ii Abstract Geographic ranges of species are fundamental units of study in ecology and evolutionary biology, since they summarize views of how species’ populations and individuals are organized in space and time. Here, I assess how abiotic and biotic factors limit and constrain species’ geographic range, structure its distributions, and change in importance at multiple spatial and temporal scales. I approach this challenge using models and testable hypothesis frameworks in the context of ecological, geographic, and historical conditions. Concentrating on a single species, the desert mistletoe, Phoradendron californicum, I assess the relative importance of factors associated with dispersal, host-parasite-vector niche overlap, and phylogeographic patterns for cpDNA within a 6 mya timeframe and at local-to-regional geographic extents. Results from a comparison of correlative and process-based modeling approaches at resolutions 1-50 km show that dispersal-related parameters are more relevant at finer resolutions (1–5 km), but that importance of extinction-related parameters did not change with scale. Here, a clearer and more comprehensive mechanistic understanding was derived from the process-based algorithm than can be obtained from correlative approaches. In a range-wide analysis, niche comparisons among parasite, hosts, and dispersers supported the parasite niche hypothesis, but not alternative hypotheses, suggesting that mistletoe infections occur in non-random environmental subsets of host and disperser ecological niches, but that different hosts get infected under similar climatic conditions, basically where their distributions overlap that of the mistletoe. In a study of iii 40 species, including insects, plants, birds, mammals, and worms distributed across the globe, genetic diversity showed a negative relationship with distance to environmental niche centroid, but no consistent relationship with distance to geographic range center. Finally, P. californicum’s cpDNA phylogenetic/phylogeographic relationships were most probable under a model of geologic events related to formation of the Baja California Peninsula and seaways across it in the Pliocene and the Pleistocene; however, fossil record, niche projections to the LGM, and haplotype distribution suggested shifting distributions of host-mistletoe interactions and evidence of host races, which may explain some of the genealogical history of the cpDNA. In sum, the chapters presented here provide robust examples and methodologies applied to estimating the importance and scale at which different sets of abiotic and biotic factors act to structure a species’ geographic range. iv Acknowledgements I wish to express my deepest gratitude to all of those who helped me throughout this learning experience. I am indebted to my advisors Jorge Soberón and A. Townsend Peterson for their unconditional support and friendship. From them I learned not only how to think about science but about life. I am grateful to my coauthors, committee members, and collaborators, and for the scientific knowledge gained in working with them. Specifically, I wish to thank: Jorge Soberón, Curtis P. Miller, A. Townsend Peterson, Joe Manthey, Oscar Toro, Jamie Oaks, and Mark Mort. The support of my committee members throughout work on this dissertation as well as other academic activities at KU was invaluable. This includes guidance on remote sensing from Steve Egbert, on ecophysiology from Craig Martin, on molecular work from Mark Mort. I feel privileged to count myself among the collaborative team that developed from the Ecological Niche Modeling seminar. This working group has been one of the most significant components of my academic exercises at KU. From this group I thank Yoshinori Nakazawa, Alberto Jiménez-Valverde, Sean Maher, Narayani Barve, Vijay Barve, Mona Papeş, Erin Saupe, Cori Myers, Hannah Owens, and Peter Hosner. I also want to give special thanks to my friends and colleagues Victor Baruch, Lindsay Campbell, Jesse Grismer, Carl Oliveros, Cam Siler, Charles Linkem, and Fabricio Villalobos. For their contributions to the fieldwork research presented in chapter 1, I am grateful to Luis A. Sánchez-González, Gerardo Cendejas, Fran Recinas, and Rebecca v Crosthwait. I wish to thank the personnel from several institutions and herbaria where we stored specimens: Socorro González (Centro Interdisciplinario de Investigaciones para el Desarrollo Integral Regional, Durango), Hilda Flores (Instituto de Biología, UNAM), José Delgadillo (Universidad Autónoma de Baja California, Ensenada), and Jon Rebman (San Diego Natural History Museum). I thank the curators and staff of the following herbaria for providing access to their digital data: ARIZ, ASC, ASU, BCMEX, BNHM, CANB, COCHISE, DES, GBIF, GCNP, IZTA, KANU, LL, MABA, MO, NMBCC, NY, RM, SNM, TEX, UCR, UNM, USON, UTC, UVSC, XAL. I thank Luis Eguiarte and Mark Olson for help with logistics, and the families of Gela and Alberto Búrquez, Sharon Herzka and Juan Pablo Lazo, Socorro González, Gerardo Cendejas, and Rebecca Crosthwait for their warm hospitality. Initial discussions about this work with Carlos Martínez del Río and statistical guidance from Exequiel Ezcurra were crucial. I also thank A. Townsend Peterson for insightful comments on this work and Narayani Barve for help with weather values interpolation. Conversations with Richard Felger and Mark Robbins were important to clarify points on climatic limiting factors and dispersal of the species. For the work related to chapter 2 I thank Sean Maher for guidance on niche overlap estimates, Mark Robbins for advice on potential mistletoe bird dispersers, Richard Felger for help with species identifications and valuable comments on background areas, and Ben Wilder for valuable comments on the manuscript. For their comments on chapter 3, I thank John K. Kelly, Jorge Soberón, A. Townsend Peterson, Lindsay P. Campbell, Jose Alexandre F. Diniz-Filho and three anonymous reviewers who helped us to improve previous versions of this manuscript. vi For their contributions to chapter 4 I thank Ben Wilder for obtaining samples from Isla del Tiburón and Isla Ángel de la Guarda; Richard Felger and Pedro Peña for help with regionalization of the Sonoran Desert; and Jenny Archibald and Farzana Ahmed for help with lab work and DNA extractions. Comments from A. Townsend Peterson, Richard Glor, and Emily McTavish helped to improve previous version of the manuscript. I thank curators from ASU for permission to sample loaned specimens as well as Craig Freeman and Caleb Morse from KANU for supporting this project. Scholarship support from Consejo Nacional de Ciencia y Tecnología, Mexico (189216) enabled me to finance the first four years of studies at KU. Collecting trips were possible thanks to financial support from a University of Kansas Biodiversity Institute Panorama small grant award (Bunker Fund), a Tinker Award from the University of Kansas Center of Latin American Studies, a Young Researchers Award from the Global Biodiversity Information Facility (GBIF). Living expenses were also provided by a scholarship from Secretaría de Educación Pública, Mexico, a Summer Research grant in 2013 from the KU Department of Ecology & Evolutionary Biology, and grants from JRS Biodiversity Foundation and the Instituto de Ecología, Xalapa, México (SAGARPA-IICA-INECOL 2013). An Interdisciplinary Seed Grant from The Commons gave me the opportunity to participate in one of the most enriching experiences—a multidisciplinary research project with Ford Ballantyne IV, Donald Worster and Jorge Soberón. Participation in conferences was possible thanks to financial support from the KU Department of Ecology and Evolutionary Biology, the KU Office of Graduate Studies, the KU Biodiversity Institute, the National Science Foundation’s IGERT Program at KU, vii and the Next Generation Sonoran Desert Researchers. A Marcia Brady Tucker Student Travel Award funded travel to present research at the 127th AOU Meeting. KU offered the best possible environment for this dissertation. Special thanks to my friends Quica and Esteban Lerner, Monica Papeş and Arpi Nyari, the Lira-Noriega foundation, the Campbell, Soberón and Peterson families, and Emily Ryan for their support. viii Table of Contents Abstract ............................................................................................................................... iii Acknowledgements .............................................................................................................