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The Pennsylvania State University the Graduate School Eberly College of Science PHYLOGENETICS, POPULATION GENETICS and ECOLOGY T

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The Pennsylvania State University the Graduate School Eberly College of Science PHYLOGENETICS, POPULATION GENETICS and ECOLOGY T The Pennsylvania State University The Graduate School Eberly College of Science PHYLOGENETICS, POPULATION GENETICS AND ECOLOGY TO UNDERSTAND THE EVOLUTION OF CORAL-ALGAL MUTUALISMS A Dissertation in Biology by Jorge H. Pinzón © 2011 Jorge H. Pinzón Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy May 2011 The dissertation of Jorge H. Pinzón was reviewed and approved* by the following: Andrew Stephenson Professor of Biology and Assistant Department Head for Research Chair of Committee Todd C. LaJeunesse Assistant Professor of Biology Dissertation Adviser Iliana Baums Assistant Professor of Biology David Geiser Professor of Plant Pathology Douglas Cavener Professor and Head of Biology *Signatures are on file in the Graduate School. ii ABSTRACT Scleractinian corals form mutualistic associations with dinoflagellates in the genus Symbiodinium. This association has allowed scleractinians, over geological time, to create the framework of one of the most diverse and productive ecosystems on the planet; the coral reefs. While major environmental changes appear to have caused significant changes in partner combinations, there is considerable data to indicate that co- evolutionary processes lead to high host-symbiont specificity and possibly speciation. The study of coral-Symbiodinium associations can be use to understand processes of speciation and the relative importance of biotic (host-specialization) and abiotic factors (isolation by distance, environmental extremes) in the evolution and diversification of both symbiotic partners. The objective of this dissertation is to elucidate the ecological and environmental/geographic factors that are important in the co-evolution of coral-algal mutualisms and how these interactions result in the formation of specific associations and the diversification of corals and algae. The first part of the dissertation is focused on examining the genetic diversity of corals in the genus Pocillopora throughout the Indo- Pacific Ocean and how their symbionts differ with regard to the genetic identity of the animal in combination with geographic location and regional environmental conditions. The second part is designed to assess the influence of host identity and geography on the gene flow among populations of Symbiodinium fitti in the Caribbean. Pocillopora is a common coral genus widely distributed throughout the Indo- Pacific Ocean and the Red Sea. Pocillopora spp. are major reef building corals in the large, isolated Tropical Eastern Pacific (TEP) region. Shallow coral communities in the TEP extend from the Gulf of California to Ecuador. Approximately seven cosmopolitan (P. damicornis, P. verrucosa, P. meandrina, P. ligulata, P. woodjonesi. P. eydouxi and P. capitata) and two endemic (P. effusus and P. inflata) species of Pocillopora recognized based on morphology are found in the TEP. Many species within the genus are phenotypically plastic to the extent that colony and branch morphology between different species may overlap creating uncertainty in their taxonomy. To examine this diversity more carefully (Chapter One), genetic analyses using nuclear (ITS2) and mitochondrial (ORF) DNA sequence data, and microsatellite markers were employed to investigate species boundaries. Colonies were collected at several locations over a broad latitudinal range throughout the TEP (Sea of Cortez, Banderas Bay and Oxaca in Mexico, Clipperton Atoll, Panama and Galapagos). The results identified only three distinct genetic entities of Pocillopora that do not corresponded to morphology. The most common genetic type, designated Type 1, was found throughout the entire region. A second type (Type 3) was identified in equatorial regions (Panama and Galapagos) and a third (Type 2), most likely a rare endemic, occurred only at the isolated Clipperton atoll. Each of these genetic “types” associated with different species of symbiont: Type 1 associated with Symbiodinium C1b-c and S. glynni, Type 3 with S. C1d-c and Type 2 with S. C1ee. Genetic, ecological and biogeographic analyses suggested the diversity of Pocillopora in the TEP is less than previously defined exclusively on macromorphological features (i.e. colony size and branching patterns). Based on these iii findings, it appears that two of the three species are potentially susceptible to climate change, as they do not associate with the thermally tolerant S. glynni. Contradictions between morphologically defined species and their genetic make up in Pocillopora from the TEP indicated the need for a major revision of the taxonomic status of Pocillopora spp. In an attempt to assess the diversity of the genus Pocillopora (Chapter Two), collection and analyses of samples from various locations in the Pacific (Hawaii, Australia, Thailand, Palau and Taiwan) and Indian Ocean (Tanzania) were performed. The results indicate Pocillopora is composed of at least eight well-defined species with little or no correspondence to morphological features. Inconsistencies between morphology and genetics led to revise the taxonomy for the Pocillopora. Accurate species delineations are important to understand the biology, ecology and evolution of life as well as to improve conservation. An example of this is presented by studying the clonal and reproductive structure of Pocillopora type 1 from two close coral communities in the Gulf of California, off La Paz, Mexico (Chapter Three). Microsatellite loci data analyses revealed that although gene flow is present, P. type 1 has a different reproductive structure on each reef. The exposed reefs, with more high action and a wider platform, is dominated by sexual reproduction while the enclosed, more protected area is highly clonal. Although comparisons with previous studies are not possible (i.e. different methodologies or molecular markers), both reproductive strategies have been found in Pocillopora and none seems related to marginality of the populations. Host selection leads to the diversification of specialized symbiont populations and can be an important step in sympatric speciation. Species radiations in at least two identified Symbiodinium clades (B and C) suggested the diversity of the group alternates between low (mostly generalist) and high (mostly specialist) number of species. Symbiodinium clade A showed a similar pattern of species diversification. Analysis of 10 microsatellite loci showed structured populations of Symbiodinium fitti harbored by different coral hosts (Chapter four). Populations found in Stephanocoenia intersepta were genetically different from those harbored by Acropora species. Among Acropora spp, symbiont populations were not completely isolated from each other with some clonal lines present in both A. palmata and A. cervicornis. Analyses of populations harbored by the same host at different locations showed geographical isolation between S. fitti populations from different locations (Colombia, Panama and Mexico). Symbiodinium speciation seems to be driven by a combination of host selection and environmental/geographical isolation. The conclusions of this research are: (1) information from the dinofalgellate algae can be use to delineate coral species in combination with phylogenetic and population genetic analyses of the host. (2) Coral-algal associations change over geographical ranges suggesting a geographical mosaic of co-evolution with host populations widely distributed and symbiont populations more isolated. (3) Sympatric coral species effectively reduce gene flow between populations of Symbiodinium, and (4) Host identity is a major factor in the diversification of Symbiodinium species. iv TABLE OF CONTENTS LIST OF TABLES.............................................................................................................................................vii LIST OF FIGURES..........................................................................................................................................viii ACKNOWLEDGEMENTS ............................................................................................................................xiii INTRODUCTION ............................................................................................................................................... 1 CHAPTER 1: SPECIES DELIMITATION OF COMMON REEF CORALS IN THE GENUS POCILLOPORA USING NUCLEOTIDE SEQUENCE PHYLOGENIES, POPULATION GENETICS, AND SYMBIOSIS ECOLOGY ................................................................................................. 5 Abstract ............................................................................................................................................................. 5 Introduction....................................................................................................................................................... 6 Methods ........................................................................................................................................................... 10 Results.............................................................................................................................................................. 18 Discussion ....................................................................................................................................................... 27 References ....................................................................................................................................................... 40 CHAPTER
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