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MECHANISMS and GENOMIC PATTERNS of REPRODUCTIVE ISOLATION in XIPHOPHORUS FISHES a Dissertation by RONGFENG CUI Submitted To

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MECHANISMS AND GENOMIC PATTERNS OF REPRODUCTIVE ISOLATION IN XIPHOPHORUS FISHES A Dissertation by RONGFENG CUI 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, Adam G. Jones Michael Smotherman Spencer T. Behmer Head of Department, Thomas McKnight May 2014 Major Subject: Biology Copyright 2014 Rongfeng Cui ABSTRACT Learned mate choice has a fundamental role in population dynamics and speciation. Social learning plays a ubiquitous role in shaping how individuals make decisions. Learning does not act on a blank slate, however, and responses to social experience depend on interactions with genetically-specified substrates – the so-called “instinct to learn”. I develop a new software Admixsimul, which allows forward-time simulations of neutral SNP markers and functional loci, mapped to user-defined genomes with user-specified functions that allow for complex dominance and epistatic effects. Complex natural and sexual selection regimes (including indirect genetic effects) are available through user-defined, arbitrary fitness and mate-choice probability functions. Using simulation, I show that responses to learned stimuli can evolve to opposite extremes in the context of mating decisions, with choosers either preferring or avoiding familiar social stimuli, depending on the relative importance of inbreeding avoidance versus conspecific mate recognition. I also show that under certain scenarios, learned preference is sufficient to maintain reproductive isolation during secondary contact. Two sister species of swordtail fish have evolved such opposite responses to learned social stimuli. The interaction of learned and innate inputs in structuring mate- choice decisions can explain variation in genetic admixture in natural populations. Olfactory preference of X. malinche females is affected by previous experience with adult cues. I compare gene expression levels of transcriptome libraries prepared from pooled sensory and brain tissues between 3 treatment groups that differ by social ii experience. I found genes involved in neural plasticity differentially expressed not only between control and exposure groups, but also between groups exposed to conspecific and heterospecific models. I also found evidence that certain vomeronasal receptor type 2 (V2R) paralogs may detect species-specific pheromone components and show differential expression between treatment groups. I then reconstruct evolutionary relationships among swordtails and platyfishes (Xiphophorus: Poeciliidae). Using genomic data, I resolve a high-confidence species tree of Xiphophorus that accounts for both incomplete lineage sorting and hybridization. The results allow me to re-examine a long-standing controversy about the evolution of the sexually selected sword in Xiphophorus, and demonstrate that hybridization has been strikingly widespread in the evolutionary history of this genus. iii DEDICATION To my grandparents, parents and family To my childhood friends. To my teachers. iv ACKNOWLEDGEMENTS My dissertation study would have not been possible without the unconditional help and mentorship from my advisor Prof. Gil Rosenthal. He not only taught me knowledge related to his expertise, but also instilled me with optimistic (and calorious) energy throughout my training. I thank my committee members Prof. Adam Jones, Prof. Mike Smotherman and Prof. Spencer Behmer for guiding the path of my study and providing constructive ideas. Prof. Mariana Mateos & Prof. Jim Woolley taught me phylogenetics, and generously helped me gain access to the TAMU Brazos cluster, where I conducted most of the computational work. I am indebted to my collaborators Machteld Verzijden, Molly Schumer and Prof. Peter Andolfatto for working with me on sexual imprinting and high-throughput genomics. I also thank my undergraduate assistant Michael Stanley for his hard work. Benjamin Philmus, Prof. Jim Smith, Prof. Prof. Larry Dangott and Prof. Yohannes Rezenom have provided generous assistance and equipment in an early project in pheromone characterization. During the past five years I have received much help and moral support in study and life from many great friends and colleagues in the department, including Prof. Charles Criscione, Prof. Leslie Winemiller, Dr. Kay Goldman, Dr. Brad Johnson, Dr. Zach Culumber, Dr. Holly Kindsvater, Dr. Clay Small, Dr. Jill Detwiler, Dr. Michi Tobler, Dr. Kim Paczolt, Dr. Nick Ratterman, Courtney Passow, Olivia Ochoa, Melissa Giresi, Emily Rose, Emily Kasl, Mitchell Ramsey, Ying Fang, Nehemiah Cox, Sehresh v Saleem, Amrita Sherlekar, Victoria Smith, Huinan Li, Pablo Delclos, Mattie Squire, Sarah Flanagan, Dan Powell, Gastón Jofre and Laura Edelstein. My work is supported by an NSF DDIG and a Rosemary Grant from S.S.E. I also received travel grants from TAMU Neuroscience, and SICB. As a boy growing up in a large, economic-driven city Canton, I am fortunate enough to pursue my childhood dream of becoming an animal biologist, a rather outlandish career in the culture, thanking to the support and love of my parents and my grandparents. I thank my childhood friends, Mingkai Liu, Yue Zhuo, Yaqi Lin among many others, who have embraced my love for animals. I am also indebted to many outstanding educators, whose names I cannot fully list below, during my K-12 and college education. They have encouraged, equipped and helped me to develop my interest into a career path: Ms. An Zhang (maths), Ms. Yingpei He (Chinese), Mr. Hua Shen (Chinese), Ms. Xin Chen (biology), Ms. Shaoming Liu (biology), Mr. Jianrong Yi (biology), Ms. Jufen Zeng (chemistry), Wendy Lan (English), Aaron Yao (English), Mr. Yingyong Wang (undergraduate advisor) and Prof. Zhaorong Lun (undergrad. co- advisor). Finally, with this work I would like to commemorate my beloved grandma, who seeded my interest in animal diversity, and passed away 55 days before my defense. vi TABLE OF CONTENTS Page ABSTRACT ....................................................................................................................... ii DEDICATION .................................................................................................................. iv ACKNOWLEDGEMENTS ............................................................................................... v TABLE OF CONTENTS ................................................................................................. vii LIST OF FIGURES ........................................................................................................... ix LIST OF TABLES ........................................................................................................... xii CHAPTER I INTRODUCTION ....................................................................................... 1 CHAPTER II EVOLUTION OF REVERSED HEDONIC VALUE IN LEARNED MATING PREFERENCES ................................................................................................ 7 Introduction ................................................................................................................ 7 Materials and methods ................................................................................................ 9 Results and discussion .............................................................................................. 19 Conclusions .............................................................................................................. 28 CHAPTER III EARLY LEARNING TRIGGERS EXPRESSION CHANGES IN NEURAL PLASTICITY GENES AND ODORANT RECEPTORS IN XIPHOPHORUS MALINCHE ......................................................................................... 30 Introduction .............................................................................................................. 30 Methods .................................................................................................................... 34 Results ...................................................................................................................... 40 Discussion ................................................................................................................ 48 Conclusions .............................................................................................................. 53 CHAPTER IV PHYLOGENOMICS REVEALS EXTENSIVE RETICULATE EVOLUTION IN XIPHOPHORUS FISHES ................................................................... 54 Introduction .............................................................................................................. 54 Methods .................................................................................................................... 59 Results ...................................................................................................................... 71 vii Discussion ................................................................................................................ 78 Conclusions .............................................................................................................. 84 CHAPTER V CONCLUSIONS ...................................................................................... 86 REFERENCES ................................................................................................................. 90 APPENDIX A ...............................................................................................................
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