MECHANISMS OF ADAPTATION IN CORAL SNAKE MIMICRY David William Kikuchi A dissertation submitted to the faculty of the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Biology. Chapel Hill 2013 Approved by: David W. Pfennig Allen H. Hurlbert Karin S. Pfennig Maria R. Servedio Kyle Summers ©2013 David William Kikuchi ALL RIGHTS RESERVED ii ABSTRACT DAVID WILLIAM KIKUCHI: MECHANISMS OF ADAPTATION IN CORAL SNAKE MIMICRY (Under the direction of David Pfennig) In Batesian mimicry, an undefended prey species (the mimic) evolves to resemble a defended one (the model) because of the selective advantage of this resemblance in deterring predation. Although Batesian mimicry is one of the oldest known examples of natural selection’s power to produce adaptation, many unanswered questions remain about its evolution, including how mimetic signals coevolve with the perceptual abilities of predators, how mimetic signals are produced, how important shared evolutionary history with a model species is for mimics, and if mimicry can evolve over rough adaptive landscapes. My thesis attempts to address these knowledge gaps by examining the venomous coral snake Micrurus fulvius and its nonvenomous mimic, the scarlet kingsnake Lampropeltis elapsoides. In addition to my empirical studies, I have produced two reviews: one is a general review of mimicry in the form of an annotated bibliography, and the other a review of the hypotheses for imperfect mimicry. In a field experiment, I asked whether or not predators were sensitive to differences between models and mimics in phenotype, that is to say, imperfect mimicry. iii My results revealed that imperfect mimicry was tolerated in some dimensions but not others, and that predators’ cognitive biases play a role in perpetuating imperfect mimicry. Two analytical studies of snake pigmentation revealed that coral snakes, their mimics, and several nonmimetic snakes use the same structures and pigments to produce their coloration. The spectral properties of colors produced by those pigments produce similar perceptual experiences for likely agents of selection in coral snake mimicry. This suggests that sharing developmental systems may facilitate the evolution of mimicry. In another field experiment I tested the assumption that the adaptive landscape between mimicry and crypsis (from which mimicry is thought to evolve) is always rough, featuring an “adaptive valley” of selection against intermediate phenotypes. Under ecological conditions that produce strong selection for precise mimicry, intermediate phenotypes were selected against; however, this was not the case when selection for mimicry was less intense. Therefore, the assumption that the evolution of mimicry always involves a transition through maladaptive intermediate phenotypes may be unwarranted. iv ACKNOWLEDGMENTS Without the contributions of many individuals besides myself, this thesis would never have been finished. I would like to thank my advisor for his objective yet unstintingly enthusiastic involvement with my projects, and my thesis committee for their feedback on the ideas we produced. The many people who have been associated with the Pfennig labs gave me critical advice on everything from statistics to the practicalities of being a graduate student, and indispensable help with experiments. The much larger, less easily defined community of the UNC Biology Department made no less valuable contributions by creating an atmosphere of intellectual curiosity that perpetually fostered new insight. Thanks to my friends for their support, tolerance, and laughter during these five years of reconciling a bunch of abstract notions with the natural world. And most of all, thank you to my family for your unconditional love, without which none of this would mean a thing. v CHAPTER ACKNOWLEDGMENTS Chapter III: We thank K. Pfennig, R. Martin, J. Santos, C. Ledón-Rettig, S. Dhole, A. Leichty, L. Bono, J. Paull, J. Weiss, M. Edmunds, and an anonymous reviewer for helpful comments, and A. Bailey, S. Clarke, and W. Juliantius for lab assistance. This work was funded by the US National Science Foundation and Sigma Xi. All procedures complied with applicable state and US federal regulations. Chapter IV: We thank Karin Pfennig, Verónica Rodriguez-Moncalvo, Lisa Bono, and three anonymous referees for helpful comments. Antonio Serrato helped with specimen collection. Chris Willett and Erin Burch aided with spectroscopy, and Vicky Madden and Steven Ray provided TEM services. Ken Wray kindly furnished coral snake specimens. Animal research was conducted under UNC IACUC permit 11-108. Funding was provided by the National Science Foundation (DEB-1110385 and DEB-1019479). Chapter V: We thank Audrey Kelly, Steve Mullin, Karin Pfennig, Antonio Serrato, Lisa Wünch, and the instructors and students in the herpetology class at SWRS for help in the field. This work was supported by NSF grants 1110385 and 1019479 and the Royster Society of Fellows at UNC-Chapel Hill. Snake collections were licensed under Arizona Game and Fish Scientific Collecting Permit #D12206055. All procedures were carried out in compliance with the Institutional Animal Care and Use Committee at UNC-Chapel Hill, under application #11-108. vi Chapter VI: We thank K. Pfennig, R. Martin, A. Leichty, J. Weiss, and two anonymous reviewers for helpful comments. Y. Choi, E. Christenson, S. Clarke, R. Searles, and G. Zhang assisted in the lab and field. The North Carolina State Museum of Natural Sciences furnished preserved specimens used in this study. This work was funded by the US National Science Foundation and a Theodore Roosevelt Memorial Grant. All procedures complied with applicable state and US federal regulations. Chapter VII: Our work has been supported by NSF grants DEB-1110385 and DEB- 1019479 and the Royster Society of Fellows at UNC-Chapel Hill. We would like to thank two anonymous reviewers for helpful comments. vii TABLE OF CONTENTS LIST OF TABLES....................................................................................................................xi LIST OF FIGURES.................................................................................................................xii CHAPTER I. GENERAL INTRODUCTION............................................................................................1 II. MIMICRY, AN ANNOTATED BIBLIOGRAPHY................................................................5 INTRODUCTION.........................................................................................................5 GENERAL OVERVIEWS..............................................................................................6 DEFINING MIMICRY..................................................................................................7 TAXONOMIC DISTRIBUTION......................................................................................9 HISTORICAL BACKGROUND....................................................................................12 BATESIAN MIMICRY................................................................................................15 MÜLLERIAN MIMICRY............................................................................................27 FUNCTIONS OF MIMETIC SIGNALS...........................................................................30 MULTIMODAL MIMICRY.........................................................................................31 IMPERFECT MIMICRY..............................................................................................32 GENETICS OF MIMICRY...........................................................................................35 POLYMORPHIC AND SEX-LIMITED MIMICRY...........................................................38 ROLE IN SPECIATION...............................................................................................40 INFLUENCE OF RECEIVER PERCEPTION....................................................................43 viii III. PREDATOR COGNITION PERMITS IMPERFECT CORAL SNAKE MIMICRY...................47 Summary................................................................................................................47 Introduction............................................................................................................47 Methods..................................................................................................................50 Results and Discussion..........................................................................................52 IV. A BATESIAN MIMIC AND ITS MODEL SHARE COLOR PRODUCTION MECHANISMS..........................................................................................61 Summary................................................................................................................61 Introduction............................................................................................................62 Methods..................................................................................................................64 Results....................................................................................................................70 Discussion..............................................................................................................73 V. MIMICRY’S PALETTE: WIDESPREAD USE OF CONSERVED PIGMENTS IN THE APOSEMATIC SIGNALS OF SNAKES.....................................................................87