ABSTRACT Genetic color polymorphisms are common in nature, and a major challenge for evolutionary biologists has been to understand how they are maintained despite the effects of directional selection. Recent studies suggest that frequency-dependent selection may explain the persistence of intraspecific variation in color. However, it remains to be determined whether frequency-dependent selection is the most predominant (or perhaps the only) mechanism to maintain such genetically-based polymorphisms. Using a South American fish, Poecilia parae, my dissertation aims to elucidate the relative roles of natural and sexual selection in the maintenance of polymorphisms in natural populations. Poecilia parae males exhibit five distinct, Y-linked and co-occurring color morphs: (i) ‗immaculata‘, the smallest and drab-colored males that resemble juvenile females; (ii) ‗parae‘, the largest males that exhibit a striped tail and black vertical body bars that intensify during social interactions; and (iii) the blue, red, and yellow morphs that are of intermediate body size and display colorful body flanks. Field surveys indicate that the frequency of each morph remains relatively stable and consistent over multiple years. Using a combination of observational and experimental studies, accompanied by techniques that aimed to characterize the visual ecology (e.g., water light transmission, visual sensitivity) of P. parae, I found that this striking color polymorphism is maintained by a complex balance between different components of natural and sexual selection. First, males of the five color morphs employ different behavioral mating strategies (hereafter alternative mating strategies, AMSs) to maximize their reproductive success. These AMSs are also accompanied by differences in morphological traits, such as testes investment and sperm morphometry that complement the specific tactic. For instance, immaculata males are often categorized as an ‗unattractive‘ male by females, which is correlated to its phenotypical appearance (smaller and drab). However, this morph is relatively abundant. I found that immaculata males specialize in ‗sneak‘ copulations and have adaptations (i.e., larger testes and unique sperm morphology) that possibly confer a fertilization advantage during postcopulatory events, when competing with the sperm of more attractive males. My studies also indicate that females have strong mating preferences for red and yellow males, with visual predators also favoring those males as prey. These findings suggest that the antagonistic interaction between pre-mating sexual selection favoring and predation acting against the red and yellow morphs may prevent them from eliminating other color morphs from the population. In fact, the red and yellow males were consistently found to be the rarest morphs across populations. Further, despite overall preference for red or yellow males, my analysis also detected female preferences for blue males. These results suggest that the interaction between female mating preferences and predation accompanied by variation in male reproductive strategies may allow for the maintenance of complex color polymorphism in natural populations. Males of the different morphs further vary in their levels of aggressive behaviors. In a series of controlled lab experiments, I found that parae males gain successful matings by preventing other males from accessing females and/or modifying female mating preferences after test females witness successful agonistic interactions. 2 Finally, I found that the signaling environment of P. parae in nature is variable and that this contributes to temporal and spatial variation in how males are perceived by females. Although red males were typically the most conspicuous morph, blue males were sometimes more conspicuous than red males at several sampling sites. The results also revealed that an aquatic model predator is able to discriminate the same male color morphs that resulted also conspicuous for females. However, it is possible that males and females of P. parae are using parts of the background spectral that are least sensitive for predators. In conclusion, my dissertation suggests that balancing selection defined by the interaction between various episodes of selection allows for the invasion of AMSs and thus the maintenance of the male color polymorphism in P. parae. 3 THE MAINTENANCE OF MALE COLOR POLYMORPHISM IN POECILIA PARAE By Jorge L. Hurtado-Gonzales B.S. Universidad Nacional San Antonio Abad del Cusco, 1992 M.A. University of Florida, 2001 DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Biology in the Graduate School of Syracuse University May 2011 4 Copyright 2011 Jorge L. Hurtado-Gonzales All rights Reserved 5 Table of Contents CHAPTER I ........................................................................................................................ 8 PREFACE ....................................................................................................................... 8 LITERATURE CITED ............................................................................................. 18 CHAPTER II ..................................................................................................................... 24 ALTERNATIVE MATING STRATEGIES MAY FAVOR THE PERSISTENCE .... 24 OF A GENETICALLY-BASED COLOR POLYMORPHISM ................................... 24 IN A PENTAMORPHIC FISH ..................................................................................... 24 ABSTRACT .............................................................................................................. 25 INTRODUCTION .................................................................................................... 26 METHODS ............................................................................................................... 29 RESULTS ................................................................................................................. 34 DISCUSSION ........................................................................................................... 37 ACKNOWLEDGMENTS ........................................................................................ 42 LITERATURE CITED ............................................................................................. 43 TABLES ................................................................................................................... 48 FIGURE CAPTIONS................................................................................................ 51 FIGURES .................................................................................................................. 53 CHAPTER III ................................................................................................................... 59 INTERACTION BETWEEN FEMALE MATING PREFERENCES AND PREDATION MAY EXPLAIN THE MAINTENANCE OF RARE MALES IN THE PENTAMORPHIC FISH POECILIA PARAE .............................................................. 59 ABSTRACT .............................................................................................................. 60 INTRODUCTION .................................................................................................... 61 METHODS ............................................................................................................... 63 RESULTS ................................................................................................................. 71 DISCUSSION ........................................................................................................... 72 ACKNOWLEDGMENTS ........................................................................................ 77 LITERATURE CITED ............................................................................................. 78 FIGURE CAPTIONS................................................................................................ 85 FIGURES .................................................................................................................. 86 SUPPORTING ELECTRONIC MATERIALS ........................................................ 90 CHAPTER IV ................................................................................................................. 104 6 INTRASEXUAL COMPETITION FACILITATES THE EVOLUTION OF ALTERNATIVE MATING STRATEGIES IN A COLOUR POLYMORPHIC FISH ..................................................................................................................................... 104 ABSTRACT ............................................................................................................ 105 BACKGROUND .................................................................................................... 107 RESULTS ............................................................................................................... 110 DISCUSSION ......................................................................................................... 112 CONCLUSIONS..................................................................................................... 117 METHODS ............................................................................................................. 117 AUTHORS‘ CONTRIBUTIONS ........................................................................... 124 ACKNOWLEDGEMENTS ...................................................................................