Coexistence, Ecomorphology, and Diversification in the Avian Family Picidae (Woodpeckers and Allies) A Dissertation SUBMITTED TO THE FACULTY OF UNIVERSITY OF MINNESOTA BY Matthew Dufort IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY F. Keith Barker and Kenneth Kozak October 2015 © Matthew Dufort 2015 Acknowledgements I thank the many people, named and unnamed, who helped to make this possible. Keith Barker and Ken Kozak provided guidance throughout this process, engaged in innumerable conversations during the development and execution of this project, and provided invaluable feedback on this dissertation. My committee members, Jeannine Cavender-Bares and George Weiblen, provided helpful input on my project and feedback on this dissertation. I thank the Barker, Kozak, Jansa, and Zink labs and the Systematics Discussion Group for stimulating discussions that helped to shape the ideas presented here, and for insight on data collection and analytical approaches. Hernán Vázquez-Miranda was a constant source of information on lab techniques and phylogenetic methods, shared unpublished PCR primers and DNA extracts, and shared my enthusiasm for woodpeckers. Laura Garbe assisted with DNA sequencing. A number of organizations provided financial or logistical support without which this dissertation would not have been possible. I received fellowships from the National Science Foundation Graduate Research Fellowship Program and the Graduate School Fellowship of the University of Minnesota. Research funding was provided by the Dayton Fund of the Bell Museum of Natural History, the Chapman Fund of the American Museum of Natural History, the Field Museum of Natural History, and the University of Minnesota Council of Graduate Students. My work would have been impossible without the extensive collections of specimens and tissue samples housed in various natural history museums, and i the collectors, preparators, and curators who generate and maintain those collections. Tissue samples were generously provided by Janet Hinshaw at the University of Michigan Museum of Zoology, Mark Robbins at the University of Kansas Natural History Museum, and Paul Sweet at the American Museum of Natural History. For access to specimens, I thank curators and collections managers at the National Museum of National History, the Burke Museum of Natural History and Culture at the University of Washington, the University of Kansas Natural History Museum, the University of Michigan Museum of Zoology, the Slater Museum of Natural History at the University of Puget Sound, the Florida Museum of Natural History, and the US Fish and Wildlife Forensics Laboratory. I thank the woodpecker phylogeneticists who came before me for making their data available in public repositories. The computationally intensive analyses presented here were made possible by the computing resources of the CIPRES Science Gateway and the Minnesota Supercomputing Institute. Finally, I thank Amber for always being there for me, and for believing in me even when I doubted myself. I thank Owen and Theo for making life more fun every day. And I thank all of my family and friends for their constant support. ii Dedication I dedicate this dissertation to Amber, Owen, and Theo, who remind me every day what’s most important. iii Abstract Interspecific competition has well-documented effects on evolution in simple systems over short timescales. However, the effects in more complex communities, and over the timescales of continental radiations, are less clear. In this dissertation, I addressed the relationships between coexistence, morphological evolution, and diversification at multiple spatial and temporal scales, using birds in the family Picidae, which includes woodpeckers and the related piculets and wrynecks. Morphology of these birds is correlated with diet and foraging mode, allowing similarity in morphological measurements to be used as a proxy for ecological similarity. Members of Picidae occur throughout the Americas, Africa, and Eurasia, and local diversity ranges from a single species to up to 13. I first generated a phylogenetic hypothesis of Picidae, and then tested predictions from community ecology and macroevolutionary theory at the community level and across the entire global radiation of Picidae. In Chapter 1, I inferred phylogenetic relationships among ~75% of extant species of Picidae, the most comprehensive molecular phylogeny of the family to date, using publicly available sequence data augmented by targeted collection of new data. While most results matched previous findings, a few species with new molecular data were placed in unexpected regions of the tree, and several genera as currently delineated appear to be paraphyletic. Relationships within most genera and previously described tribes were well resolved, but relationships among most major clades remained unclear. A number of tightly spaced iv branching events near the base of the family were not resolved with available data. In Chapter 2, I evaluated the roles of ecological assortment of species and in situ trait evolution in driving trait distributions in communities of North American woodpeckers. I used multiple null models and metrics of community trait distributions to test for deviations from randomness in six communities including a total of 10 species. I recovered a signal of divergent displacement across all populations and all communities, suggesting local evolution away from morphologically most similar species. However, trait distributions in most individual communities did not differ from random expectations. In average size and overall morphology, one community showed evidence of species sorting for dissimilar traits. In the size-scaled shape data, I found evidence of divergent and convergent local evolution in one community each. These results suggest that trait differences are related to both species sorting and local evolution, but that other processes or a lack of statistical power prevent detection of effects in many communities. In Chapter 3, I tested for relationships between coexistence and rates and modes of diversification and trait evolution across all Picidae. I used phylogenetic comparative methods to evaluate correlations among subclades of Picidae in relevant variables. I found strong and consistent positive correlations between geographic range overlap, rates of diversification, and rates of shape evolution— but not body size or overall morphological evolution. In addition, time-dependent v models of morphological evolution and diversification fit better to subclades with greater range overlap. Taken together, these findings suggest that coexistence with similar species does affect evolution in Picidae. Shape evolution shows clear connections with coexistence in both the community-level and family-wide comparative analyses. The community analyses suggest that coexistence is the cause, rather than the consequence, of this trait evolution, as the trait changes are more spatially restricted and temporally recent than apparent coexistence among many of the species. Variation in diversification rates may be driven by other factors that covary with local diversity and evolution in body shape. Future work in this group should focus on solving the remaining puzzles in phylogenetic relationships, determining the contribution of body size and shape to competitive interactions, and understanding possible relationships of other variables with diversification, morphological evolution, and coexistence. One online supplementary file (OSF) accompanies this dissertation: a spreadsheet containing the GenBank accession numbers or other sources for the DNA sequence data used in Chapter 1. vi Table of Contents List of Tables .......................................................................................................viii List of Figures....................................................................................................... ix Chapter 1: An augmented supermatrix phylogeny of the avian family Picidae reveals uncertainty deep in the family tree ............................................................ 1 Introduction................................................................................................. 2 Materials and Methods ............................................................................... 5 Results...................................................................................................... 16 Discussion ................................................................................................ 24 Conclusions .............................................................................................. 39 Chapter 2: Both species sorting and trait evolution explain non-random trait distributions in North American woodpecker communities .................................. 48 Introduction............................................................................................... 49 Materials and Methods ............................................................................. 55 Results...................................................................................................... 73 Discussion ................................................................................................ 77 Conclusions .............................................................................................. 88 Chapter 3: Diversification and trait evolution are correlated with coexistence in the avian family Picidae....................................................................................