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Pheromonal Mechanisms of Reproductive Isolation in Xiphophorus PHEROMONAL MECHANISMS OF REPRODUCTIVE ISOLATION IN XIPHOPHORUS AND THEIR HYBRIDS A Dissertation by CHRISTOPHER HOLLAND Submitted to the Office of Graduate and Professional Studies of Texas A&M University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Chair of Committee, Gil G. Rosenthal Committee Members, Michael Smotherman Kevin W. Conway Jessica L. Yorzinski Head of Department, Thomas McKnight December 2018 Major Subject: Biology Copyright 2018 Christopher Holland ABSTRACT Pheromones play an important role in conspecific mate preference across taxa. While the mechanisms underlying the pheromonal basis of reproductive isolation are well characterized in insects, we know far less about the mechanisms underlying the production and reception of chemical signals in vertebrates. In the genus Xiphophorus, conspecific mate recognition depends on female perception of male urine-borne pheromones. I focused on interspecific differences between the sympatric X. birchmanni and X. malinche, which form natural hybrid zones as a consequence of changes in water chemistry. First, I identify the organ of pheromone production and compounds comprising chemical signals. I localized pheromone production to the testis; testis extract elicited the same conspecific preference as signals generated by displaying males. I used solid phase extraction (SPE) in combination with high performance liquid chromatography (HPLC)/ mass spectrometry (MS) to characterize pheromone chemical composition. Analyzing HPLC/MS readouts for pure peaks with high relative intensity identified two compounds of interest, which were identified according to their fraction pattern and retention times and then individually assayed for their effect on female behavior. The ability to directly measure the pheromones with paired responses of female conspecific mate recognition gives insight into what specific components are important to female mate choice. Elucidating the chemical composition of Xiphophorus signals sheds light into how communication acts as a reproductive barrier between species and how its breakdown facilitates hybridization. Next, I characterize intraspecific variation in pheromone signals. Understanding the relationship between a quantifiable male pheromone profile and measurable female response provides unique insight ii into female mate choice. I examined the variation in male morphology in X. birchmanni, and used SPE to measure changes in pheromone structure in relation to distinct morphometric traits. Lastly, I evaluate the relationship of male pheromone phenotype to population substructure. If pheromones play a role in reproductive isolation, pheromone profiles should map on to male genotype morphology. Hybrid zones vary from highly structured, with distinct birchmanni-like and malinche-like subpopulations, to highly admixed hybrid swarms. I measured pheromone profiles for individual males, I show the relationship between male morphology, pheromone profile and population structure. iii DEDICATION For, Ellen Ford. Love you forever, my mum you will be. iv ACKNOWLEDGEMENTS I would like to first thank my advisor, Dr. Gil Rosenthal; over the past 4 years he has provided me with support and guidance to navigate my time in graduate school. Sharing his knowledge on mate choice and reproductive isolation with me was pivotal in my development as a young scientist and he has provided constant feedback to all of the proposals, presentations, research and manuscripts I have worked on throughout my graduate career. I would like to thank my committee, Dr. Jessica Yorzinski, Dr. Michael Smotherman, and Dr. Kevin Conway, for their guidance and support throughout the course of this research. I would also like to acknowledge Dr. Adam Jones and Dr. Peter Sorenson for their advice and constructive research contributions. A special thanks to Jennifer Bradford, for all her support and patience with me in my advancement at Texas A&M and for all of her hard work over the years helping me throughout it all. I would not have grown or enjoyed my graduate career without my lab mates, friends and peers who provided moral and emotional support, thank you so much to: Dan Powell, Gastón Jofre-Rodríguez, Dr. Molly Schumer, Mateo García, Megan Exnicios, Stephen Bovio, Carolyn Henderson, David Saenz, Luke Bower, Chris Figgener, and McKensie Daugherty. I need to thank my squad: Mattie Squire, M.S., Dr. Sarah Flanagan, and Dr. Alejandra Malandando. The three of you have taught me so much and have been there for me through it all. I know I have made lifelong friends and am eternally grateful for you all. I need to thank my family; my mother and sister who have been my never ending support system. My companion and endless source of love, Renly, who helped get me through my graduate career with early morning walks, belly rubs, puppy kisses, and staying by my side every v late night. Finally, my best friend and life partner, Eric Murray, M.S.. Thank you for understanding me, having my back and making me laugh everyday. vi CONTRIBUTORS AND FUNDING SOURCES Contributors This work was supported by a dissertation committee consisting of my advisor, Professor Gil Rosenthal, and Professor Michael Smotherman of the Department of Biology, and Professors Jessica Yorzinski and Kevin Conway of the Department of Wildlife and Fisheries Sciences. The HPLC/MS used in Chapter I, II and III were provided by Dr. Bo Wang of the Department of Chemistry at Texas A&M University. The student independently completed all other work conducted for the dissertation. Funding sources Graduate study was supported by a grant from Animal Behavior Society and a fellowship from L.T. Jordan International Travel Foundation at Texas A&M University. vii TABLE OF CONTENTS Page ABSTRACT ……......................................................................................................................... ii DEDICATION ............................................................................................................................ iv ACKNOWLEDGEMENTS ...................................................................................................…...v CONTRIBUTORS AND FUNDING SOURCES ……............................................................. vii TABLE OF CONTENTS ……................................................................................................. viii LIST OF FIGURES ..................................................................................................................... x LIST OF TABLES ..................................................................................................................... xi CHAPTER I INTRODUCTION AND LITERATURE REVIEW............................................... 1 CHAPTER II PHEROMONAL MECHANISMS OF REPRODUCTIVE ISOLATION IN TWO HYBRIDIZING SPECIES OF XIPHOPHORUS..........................................................7 Introduction ............................................................................................................................ 7 Materials and Methods ........................................................................................................... 8 Results .................................................................................................................................. 12 Discussion ............................................................................................................................ 18 Conclusions .......................................................................................................................... 19 CHAPTER III MALE PHEROMONES CO-VARY WITH ALTERNATIVE REPRODUCTIVE STRATEGIES IN A TELEOST FISH......................................................... 21 Introduction ......................................................................................................................... 21 Materials and Methods ……................................................................................................ 24 Results ................................................................................................................................. 27 Discussion ........................................................................................................................... 32 Conclusions ......................................................................................................................... 33 CHAPTER IV PHEROMONE SIGNALS, MORPHOLOGY, AND POPULATION STRUCTURE IN NATURALLY HYBRIDIZING SWORDTAIL FISH...................................35 Introduction ......................................................................................................................... 35 Materials and Methods ........................................................................................................ 37 Results ................................................................................................................................. 39 viii Discussion ........................................................................................................................... 43 Conclusions ......................................................................................................................... 45 CHAPTER V CONCLUSIONS .............................................................................................. 46 REFERENCES ........................................................................................................................ 49 ix LIST OF FIGURES Page Figure 1- Behavioral
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