FROM GENES TO COMMUNITIES: INTEGRATIVE BIOLOGY OF ACOUSTIC INTERACTIONS IN NEOTROPICAL SINGING MICE By BRET PASCH A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2011 1 © 2011 Bret Pasch 2 To Mary and Eugénie--wise and adventurous grandmothers 3 ACKNOWLEDGMENTS I thank my wife, Kate, for her love, patience, and encouragement; our new daughter, Mary, for her vibrance; and my parents and brother for their enduring support. My advisor, Steven Phelps, inspired mechanistic approaches to animal behavior while allowing me the creative space to pursue my interests. His vision and guidance have been invaluable. Comfmittee members Jim Austin, Doug Levey, Brian McNab, and David Reed provided important perspective and insight as my dissertation evolved. I am grateful to my fellow lab members, including Dimitri Blondel, Polly Campbell, Ondi Crino, Alex Ophir, and Jorge Pino for their constructive feedback and camaraderie. I enjoyed working alongside three undergraduate students, Andreas George, Molly Phillips, and Rachel Sanford. Their passion and inquisitiveness stirred my own and enriched the research experience. I thank Ben Bolker and Craig Osenberg for their advice on experimental design and data analysis, Harvey Ramirez and Dania del Castillo for their guidance on surgical technique, and Russ Charif and Dean Hawthorne at the Bioacoustics Research Program, Cornell Lab of Ornithology for their advice on sound analysis. Finally, a warm thanks to F. Michonneau, J. Monaghan, A. Seifert, M.D. Smith, and A. Stier, for their friendship and collaborations. Research was conducted with permits from UF IACUC, the Costa Rican Ministerio del Ambiente y Energia, and the Panamanian Autoridad Nacional del Ambiente. The research was supported by grants from Sigma Xi, American Society of Mammalogists, American Museum of Natural History, Society for Integrative and Comparative Biology, Organization for Tropical Studies, University of Florida Alumni Fellowship, and National Science Foundation Doctoral Dissertation Improvement Grant # 0909769. 4 TABLE OF CONTENTS page ACKNOWLEDGMENTS .................................................................................................. 4 LIST OF TABLES ............................................................................................................ 7 LIST OF FIGURES .......................................................................................................... 8 LIST OF OBJECTS ......................................................................................................... 9 ABSTRACT ................................................................................................................... 10 CHAPTER 1 INTRODUCTION .................................................................................................... 12 2 ANDROGENS MODULATE SONG EFFORT AND AGGRESSION IN NEOTROPICAL SINGING MICE ............................................................................ 14 Background ............................................................................................................. 14 Materials and Methods ............................................................................................ 16 Study Animals .................................................................................................. 16 Surgical Procedure ........................................................................................... 16 Song Recording and Measurement .................................................................. 17 Resident-Intruder Trials .................................................................................... 18 Testosterone Radioimmunoassay .................................................................... 18 Data Analysis ................................................................................................... 19 Results .................................................................................................................... 20 Plasma Androgen Concentrations .................................................................... 20 Resident-Intruder Trials .................................................................................... 20 Singing Behavior .............................................................................................. 20 Song Parameters ............................................................................................. 20 Discussion .............................................................................................................. 22 3 ANDROGEN-DEPENDENT MALE VOCAL PERFORMANCE INFLUENCES FEMALE PREFERENCE IN NEOTROPICAL SINGING MICE ............................... 34 Background ............................................................................................................. 34 Materials and Methods ............................................................................................ 37 Generating the Population Performance Limit .................................................. 37 Androgen Manipulation .................................................................................... 38 Female Phonotaxis ........................................................................................... 39 Statistical Analyses .......................................................................................... 41 Results .................................................................................................................... 43 Population Performance Limit .......................................................................... 43 Androgenic Effects on Performance Scores ..................................................... 43 5 Female Phonotaxis ........................................................................................... 44 Discussion .............................................................................................................. 44 4 INTERSPECIFIC DOMINANCE VIA VOCAL INTERACTIONS MEDIATES ALTITUDINAL ZONATION IN NEOTROPICAL SINGING MICE ............................ 53 Background ............................................................................................................. 53 Materials and Methods ............................................................................................ 56 Altitudinal Replacement Zones and Temperature Regimes ............................. 56 Interspecific Behavioral Trials ........................................................................... 57 Reciprocal Removal Experiment ...................................................................... 57 Field Playback Experiments ............................................................................. 58 Laboratory Playback Experiments .................................................................... 59 Statistical Analyses .......................................................................................... 60 Results .................................................................................................................... 61 Altitudinal Replacement Zones ......................................................................... 61 Interspecific Behavioral Trials ........................................................................... 62 Reciprocal Removal Experiment ...................................................................... 62 Field Playback Experiments ............................................................................. 63 Laboratory Playback Experiments .................................................................... 63 Discussion .............................................................................................................. 64 Role of Acoustic Communication in Interspecific Interactions .......................... 68 Conclusion ........................................................................................................ 69 5 AGONISTIC CHARACTER DISPLACEMENT IN SOCIAL COGNITION IN A TROPICAL MOUSE ................................................................................................ 77 Background ............................................................................................................. 77 Materials and Methods ............................................................................................ 79 Reciprocal Playback Experiments .................................................................... 79 Tissue Preparation ........................................................................................... 80 Egr-1 Immunocytochemistry ............................................................................. 81 Analysis of Egr-1 Immunoreactivity .................................................................. 81 Statistical Analyses .......................................................................................... 82 Results .................................................................................................................... 82 Discussion .............................................................................................................. 83 6 CONCLUSIONS ..................................................................................................... 87 LIST OF REFERENCES ............................................................................................... 92 BIOGRAPHICAL SKETCH .........................................................................................