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Mismatched Mimics: Insights and Conundrums from the Evolutionary History of Colorful Ground Beetles

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Mismatched Mimics: Insights and Conundrums from the Evolutionary History of Colorful Ground Beetles Mismatched Mimics: Insights and Conundrums from the Evolutionary History of Colorful Ground Beetles by Carlos P. Munoz Ramirez A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ecology and Evolutionary Biology) in The University of Michigan 2017 Doctoral Committee: Professor Lacey L. Knowles, Chair Professor Diarmaid O'Foighil Assistant Professor Stephen A. Smith Assistant Professor Selena Y. Smith Carlos P. Munoz Ramirez [email protected] ORCID iD: 0000-0003-1348-5476 © Carlos P. Munoz Ramirez 2017 DEDICATION This dissertation is dedicated to my family—Maribel, Aleli, and Jazmin—which has been an invaluable support along these years of intense academic and human growth. ii ACKNOWLEDGMENTS I would like to thank my lab mates Rob Mazzatti, Jen-Pan Huang, Qixin He, Lucy Tran, Andrea Thomas, and Tristan McKnight, for their insightful discussions and conversations that allowed me to learn in an enjoyable and stimulating environment. I am also thankful with my advisor, Lacey Knowles, who supported me in the most difficult moments. I learnt a great deal of good science during our conversations and lab meetings. I also want to thank Alvaro Zuñiga, Dusan Boric, Gustavo Valenzuela, Christian Muñoz, Laurent Rataj, and Dr. Viviane Jerez for donating specimens. I am especially grateful to Alvaro Zuñiga, Christian Muñoz, Alfonso Jara, Luis Correa, Jorge Avaria, Pablo Fuentes and many others for their selfless help in the field. I also thank Corporación Nacional Forestal (CONAF) for granting permits to sample within several National Parks (Authorization number: 024/2012), the Ammerman Fund from the Insect Division of Ruthven Museums for funding my fieldwork, and Becas Chile (CONICYT, Chile) (CM-R) and Fulbright scholarships for sponsorship and funding support. This research was aided with funds from Block Grants and Hinsdale-Walker scholarships from the department of Ecology and Evolutionary Biology and a National Science Foundation DDIG grant (DEB-1601260). iii TABLE OF CONTENTS DEDICATION ....................................................................................................... ii ACKNOWLEDGMENTS ........................................................................................ iii LIST OF FIGURES ................................................................................................. vi LIST OF TABLES .................................................................................................. xi Abstract ........................................................................................................... xiii Chapter 1: Introduction ...................................................................................... 1 Chapter 2: Mimics here and there, but not everywhere: Müllerian mimicry in Ceroglossus ground beetles? ............................................................................... 4 2.1 ABSTRACT ............................................................................................................................................................ 4 2.2 INTRODUCTION ................................................................................................................................................... 4 2. 3 METHODS ........................................................................................................................................................... 6 2.4 RESULTS ............................................................................................................................................................... 7 2.5 DISCUSSION ......................................................................................................................................................... 7 2.6 FIGURES ............................................................................................................................................................. 11 2.7 APPENDIX .......................................................................................................................................................... 13 iv Chapter 3: Coalescent species delimitation in mimetic beetles: Are color morphs different species? Does it matter for understanding the evolution of mimicry? 20 3.1 ABSTRACT .......................................................................................................................................................... 20 3.2 INTRODUCTION ................................................................................................................................................. 21 3.3 MATERIAL AND METHODS ................................................................................................................................. 25 3.4 RESULTS ............................................................................................................................................................. 31 3.5 DISCUSSION ....................................................................................................................................................... 34 3.6 TABLES ............................................................................................................................................................... 41 3.7 FIGURES ............................................................................................................................................................. 46 3.8 APPENDIX .......................................................................................................................................................... 50 Chapter 4: Phylogenetic tests of the role of mimicry in the diversification of mimetic ground beetles .................................................................................... 58 4.1 ABSTRACT .......................................................................................................................................................... 58 4.3 MATERIALS AND METHODS ............................................................................................................................... 62 4.4 RESULTS ............................................................................................................................................................. 68 4.5 DISCUSSION ....................................................................................................................................................... 70 4.7 TABLES ............................................................................................................................................................... 75 4.8 FIGURES ............................................................................................................................................................. 78 4.9 APPENDIX .......................................................................................................................................................... 81 Chapter 5: Conclusion ....................................................................................... 87 BIBLIOGRAPHY .................................................................................................. 90 v LIST OF FIGURES FIGURES CHAPTER 2: Figure 2.1: Colour diversity across the three Ceroglossus taxa analysed in this study. Relationships based on a Bayesian tree for COI recovered each of the three taxa as monophyletic (highlighted in grey). The * symbol indicates Bayesian posterior probabilities above 0.9. ………………………………………………………………………………………………………………………………11 Figure 2.2: (A) Distribution map of Ceroglossus beetles highlighting by reference to sampled localities for three species (ch= Ceroglossus chilensis, dar= Ceroglossus darwini group, and buq= Ceroglossus buqueti) geographic areas where the taxa co-occur (shown by pie diagrams). Colour in the pie diagrams represents approximate species colouration in that area. The small coloured dots refer to localities where only a single species was collected. (B) Boxplots showing how within-site colour distances compare to between-site distances. (C) Randomization test showing the distribution of random colour-distance means versus the empirical within-site distance mean (dashed line)………………………………………………………………………………………………………………….12 Figure S1: Analysis of the data using an avian VS visual model. (A) Comparison between different sets of distances and (B) the randomization test showing the distribution of random colour- distance means versus the empirical within-site mean (dashed line). Note that the empirical within-site mean distance between species is smaller than expected by a random distribution……………………………………………………………………………………………………………………………….18 vi Figure S2: Analysis of the data using a reptilian visual model. (A) Comparison between different sets of distances and (B) the randomization test showing the distribution of random colour- distance means versus the empirical within-site mean (dashed line). Note that the empirical within-site mean distance between species is smaller than expected by a random distribution. …....................................................................................................................................................18 Figure S3: Average spectral curve ± SE (calculated at each wavelength) of Ceroglossus chilensis, C. buqueti, and C. darwini, for seven Chilean localities where all three species are sympatric….19 FIGURES CHAPTER 3: Figure 3.1: Sample sites for three taxa of Ceroglossus ground beetles. (A), C. chilensis;
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