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Evolutionary Genetics of Pocillopora Corals

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Evolutionary Genetics of Pocillopora Corals Evolutionary Genetics of Pocillopora Corals by David J. Combosch Diploma Environmental Scientist, University Duisburg-Essen A dissertation submitted to the Faculty of the College of Science of Northeastern University In partial fulfillment of the requirements for the degree of Doctor of Philosophy December 2, 2013 Dissertation directed by Steven V. Vollmer Associate Professor of Marine & Environmental Sciences DEDICATION Für Walter Combosch ii ACKNOWLEDGEMENTS I am grateful to my advisor Steven Vollmer for his support, guidance and friendship. I thank all my committee members, Rebeca Rosengaus, Matthew Bracken, Geoff Trussell and especially Gonzalo Giribet for their support and advice and my German mentor Helmut Schuhmacher for many years of support. In addition, I want to thank many colleagues and friends from the Vollmer Lab, especially Silvia Libro, Liz Hemond, Sarah Gignoux-Wolfsohn, Chris Marks and Stefan Kaluziak as well as the Giribet Lab, especially Vanessa Gonzales and Alicia Perez-Porro and my collaborators Lauren Toth, Rich Aronson and Ian McIntyre. I benefitted greatly from the Three Sea Program, particularly due to the help of Sal Genovese, Pete Edmunds, Ruth Gates, Brian Helmuth, Josh Idjahdi, Jim Leichter and Bill Precht. Numerous friends in America, Germany, Panamá, France, French Polynesia and especially in 123 River Street contributed a lot, both directly and indirectly, to this dissertation, especially my girlfriend Sarah Lemer, my brother Florian and his family Fiona, Liva, Clara und Bruno as well as my parents Lene and Walter Combosch. This work was supported by a German Academic Exchange Service Pre-doctoral fellowship, Teaching assistantship awards from Northeastern University and the Three Seas Program and the National Science Foundation to Steven Vollmer. iii ABSTRACT OF DISSERTATION My dissertation research addresses fundamental questions about the evolution of tropical reef corals in isolated biogeographic regions. The main focus is on the effect of intra- and inter- specific gene flow within and among peripheral coral populations. Since introgression and genetic connectivity are keys factor for evolution and adaptation as well as for population resilience, recovery and persistence, the identification and quantification of past and present gene flow is of major interest, not only for basic evolutionary research but also for applied conservation. The central question of my research is the how the widespread, but generally subordinate reef-building coral Pocillopora damicornis became the ecologically dominant reef-builder in the isolated, environmentally challenging Tropical Eastern Pacific (TEP). The dominance of TEP Pocillopora damicornis populations is accompanied by strong differences in life-history traits, including a shift in reproductive strategy from brooding predominantly parthenogenetic larvae in the Indo-West Pacific to broadcast spawning in the TEP. Using a combination of genetic tools ranging from multi-locus Sanger sequencing to RAD-Seq phylogenomic analyses, I show that three genetic lineages that are found in TEP and Central Pacific P. damicornis populations are characterized by strong genome-wide differences, which suggests that they belong to separate species. However, a subset of loci was shared among P. damicornis colonies across lineages and across large geographic distances. The allelic composition of putative hybrid samples indicate repeated uniparental backcrossing and substantial genomic introgression among TEP Pocillopora species. The population genetic structure of TEP P. damicornis indicates limited gene flow among and within populations, which enables effective adaptations to the environmentally iv heterogeneous TEP environment. Predominantly sexual reproduction, significant inbreeding and small-scale spatial genetic structures over meter scales within populations further sustain divergent adaptations. This small-scale population genetic structure allows P. damicornis to adapt locally to the harsh environmental condition of the Tropical Eastern Pacific and presumably facilitated its regional dominance. In addition, I show that Central Pacific P. damicornis display a unique mixed reproductive strategy that includes the simultaneous production of sexual and asexual larvae. While the majority of larvae are produced parthenogenetically, most colonies also produce a subset of their larvae sexually. The proportion of sexually produced larvae decreases with colony size, suggesting that the mixed reproductive strategy is flexible and changes across the life of the coral, leading to an increasingly asexual propagation of locally successful genotypes. Combined, I have shown that Pocillopora corals in the peripheral TEP are characterized by interspecific gene flow between P. damicornis and its congeners P. eydouxi and P. elegans and limited gene flow among and within P. damicornis populations. I showed that the morphospecies Pocillopora damicornis is composed of multiple genetic lineages, in part due to introgressive hybridization in the TEP. Pocillopora populations further differ in their reproductive strategies with central Pacific populations reproducing predominantly parthenogenetic and TEP populations reproducing mostly sexually. v TABLE OF CONTENTS DEDICATION II ACKNOWLEDGEMENTS III ABSTRACT OF DISSERTATION IV TABLE OF CONTENTS VI LIST OF FIGURES IX LIST OF TABLES XI CHAPTER 1 - GENE FLOW, POCILLOPORA CORALS AND THE TROPICAL EASTERN PACIFIC 1 Overview 1 Gene Flow 2 Pocillopora corals 7 The Tropical Eastern Pacific 10 References 14 CHAPTER 2 - POPULATION GENETICS OF AN ECOSYSTEM-DEFINING REEF CORAL - POCILLOPORA DAMICORNIS IN THE TROPICAL EASTERN PACIFIC 25 Abstract 25 Introduction 26 Materials and Methods 30 Results 35 Discussion 38 vi Conclusion 49 Acknowledgements 50 References 51 Tables 62 Figures 67 Supplementary Material 70 Chapter 3 - MIXED ASEXUAL AND SEXUAL REPRODUCTION IN THE INDO-PACIFIC REEF CORAL POCILLOPORA DAMICORNIS 71 Abstract 71 Introduction 72 Materials and Methods 74 Results 77 Discussion 78 Conclusion 85 Acknowledgements 86 References 87 Tables 93 Figures 96 CHAPTER 4 - EVOLUTIONARY GENOMICS OF POCILLOPORA CORALS 101 Abstract 101 Introduction 102 Material and Methods 105 Results 112 Discussion 116 vii Conclusions 125 Acknowledgements 126 References 127 Tables 133 Figures 136 Supplementary Material 143 FINAL CONCLUSIONS 149 viii LIST OF FIGURES CHAPTER 2 FIGURE 1: MAP OF PANAMÁ, SHOWING THE THREE MAIN PACIFIC REGIONS AND THE SAMPLED LOCATIONS. 67 FIGURE 2: PRINCIPAL COMPONENT ANALYSIS OF POCILLOPORA DAMICORNIS POPULATIONS, CONSTRUCTED USING GENALEX 6.1. 68 FIGURE 3: SPATIAL CORRELOGRAMS OF THE SPAGEDI ANALYSIS OF SPATIAL GENETIC STRUCTURE (SGS) AMONG SPECIMEN WITHIN DISCRETE DISTANCE CLASSES. 69 FIGURE S1: RESULTS OF THE BAYESIAN CLUSTERING APPROACH IMPLEMENTED IN STRUCTURE 2.3 THAT WERE USED TO INFER THE NUMBER OF GENETIC CLUSTERS (K) IN THE MICROSATELLITE DATASET 70 CHAPTER 3 FIGURE 1: A POCILLOPORA DAMICORNIS COLONY ON THE REEF IN FRONT OF THE GUMP RESEARCH STATION IN MOOREA, FRENCH POLYNESIA 96 FIGURE 2: THE PROPORTION OF SEXUALLY PRODUCED LARVAE DECREASES AS A FUNCTION OF COLONY SIZE 97 FIGURE 3: THE PROPORTION OF SEXUALLY PRODUCED LARVAE RELEASED DECREASES DURING THE REPRODUCTIVE CYCLES OF P. DAMICORNIS COLONIES 99 CHAPTER 4 FIGURE 1A: POCILLOPORA ELEGANS COLONY IN A P. DAMICORNIS CARPET IN ISLA COIBA, GULF OF CHIRIQUÍ, PANAMÁ. 136 FIGURE 1B: PHENOTYPIC PLASTICITY OF P. DAMICORNIS/P. VERRUCOSA IN MOOREA, FRENCH POLYNESIA. 137 ix FIGURE 2: ORF AND ITS PHYLOGENY 138 FIGURE 3: RAD PHYLOGENOMIC ANALYSES 140 FIGURE 4: PRINCIPAL COORDINATE ANALYSIS OF PAIRWISE P-DISTANCES BETWEEN RAD-SEQ SAMPLES. 141 FIGURE 5: ALLELE COMPOSITION OF PUTATIVE HYBRID P. DAMICORNIS SAMPLES COMPARED TO THE EXPECTED ALLELE COMPOSITIONS OF BACKCROSSING HYBRIDS OVER SEVERAL GENERATIONS. 142 FIGURE S1: BASIC RAD LOCI CORRELATIONS 147 FIGURE S2: PAIRWISE P-DISTANCE COMPARISONS BETWEEN SAMPLES AT TRANSCRIBED VS. UNTRANSCRIBED LOCI. 148 x LIST OF TABLES CHAPTER 2 TABLE 1: POPULATION GENETIC INDICES FOR THE SIX MICROSATELLITE LOCI. 62 TABLE 2: POPULATION GENETIC INDICES FOR THE NINE POPULATIONS. 63 TABLE 3: HIERARCHICAL AMOVA RESULTS 64 TABLE 4: PAIRWISE RST AND FST BETWEEN TEP P. DAMICORNIS POPULATIONS 65 TABLE 5: POCILLOPORA DAMICORNIS POPULATION GENETIC SURVEY (SORTED BY FST). 66 CHAPTER 3 TABLE 1: LOCI-SPECIFIC STATISTICS FOR EACH OF THE SIX SAMPLED MICROSATELLITE LOCI. 93 TABLE 2: LIST OF MATERNAL COLONIES 94 TABLE 3: RESULTS OF THE GENERALIZED LINEAR MIXED EFFECTS MODEL FOR THE MAIN LOGISTIC REGRESSION ANALYSIS 95 CHAPTER 4 TABLE 1: OVERVIEW OF THE RAD-SEQ SAMPLE COMPOSITION AND BASIC POPULATION GENETIC INDICES. 133 TABLE 2: PAIRWISE COMPARISONS BETWEEN SAMPLES USING P-DISTANCE AND IBS- PROPORTIONS. 134 TABLE 3: GENETIC MAKE-UP OF PUTATIVE HYBRID P. DAMICORNIS SAMPLES 135 TABLE S1: READ DEPTH PER SAMPLE AND PER LOCUS 143 xi TABLE S2: TRANSCRIPTOME MATCHES/ALIGNMENTS. 144 TABLE S3: IBS & NUMBER OF DIFFERENTLY FIXED LOCI 145 TABLE S4: VICE VERSA COMPARISON OF ALLELIC IDENTITY 146 xii Evolutionary Genetics of Pocillopora Corals CHAPTER 1 GENE FLOW, POCILLOPORA CORALS AND THE TROPICAL EASTERN PACIFIC Overview This dissertation explores the patterns and consequences of gene flow for the evolution of reef-building corals. Each chapter highlights a different aspect of gene flow, within species, between generation and across species. Gene flow acts on many different levels and in different, sometimes contradictive ways, to shape the genetic identity and delimitations of species and
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