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Diversity, Stability and Connectivity of Symbiodinium Populations at Various Spatial Scales

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The Pennsylvania State University The Graduate School Eberly College of Science Diversity, Stability and Connectivity of Symbiodinium Populations at Various Spatial Scales A Dissertation in Biology by Daniel T. Pettay © 2011 Daniel T. Pettay Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy August 2011 The dissertation of Daniel T. Pettay was reviewed and approved* by the following: Todd C. LaJeunesse Assistant Professor of Biology Dissertation Adviser Stephen W. Schaeffer Associate Professor of Biology Chair of Committee Andrew F. Read Professor of Biology Timothy C. Reluga Assistant Professor of Mathematics Douglas R. Cavener Professor of Biology Department Head of Biology *Signatures are on file in the Graduate School ii ABSTRACT Coral-algal symbioses construct and maintain entire ecosystems, making symbiotic dinoflagellates (Symbiodinium) among the most abundant microbial eukaryotes found on coral reefs. Despite decades of research on these associations the genotypic diversity, dispersal and population differentiation of Symbiodinium, along with the fine-scale dynamics between populations of hosts and their endosymbionts, remain unclear. Modern population genetic approaches can elucidate these patterns and substantially advance our understanding of these associations. Coral bleaching is the loss of endosymbiotic dinoflagellates due to physiological stress, such as changes temperature or light. Bleaching can lead to disease outbreaks and mass mortality and has caused widespread degradation of many reef coral communities. However, some host-symbiont combinations show higher resistance to these perturbations and their proliferation has the potential to influence the response of reef communities to climate change. Symbionts of the phylogenetic grouping Clade D represent the best known and most geographically widespread example, where host colonies associating with these symbionts exhibit tolerance to physiological stress. Given the predicted changes in the global climate, a better understanding these stress-tolerant symbionts is imperative to understanding the future of coral reef ecosystems. From a population perspective, the migration and dispersal of thermally tolerant species may influence how algal-coral symbioses respond to climate warming. To address our lack of knowledge the population processes of two species belonging to clade D were studied, the pan-Pacific species Symbiodinium glynii (D1) and the globally distributed Symbiodinium trenchii (D1a). S. glynni associates exclusively with Pocillopora spp. (i.e., host specialist) ranging from the Eastern Pacific, where the symbiosis is regionally abundant and the predominant reef- builder, to the Western Pacific and Gulf of Thailand. In contrast, S. trenchi associates with a large diversity of invertebrates in the Western Atlantic, Indian and Pacific Oceans. The intra-colony diversity, prevalence and stability of S. glynni multilocus genotypes in association with populations of Pocillopora from two sites in the Gulf of California was investigated by applying microsatellite markers developed for both host and symbiont. The genetic diversity and allelic frequencies in reef populations of S. glynni remained stable over time, with common clone lineages persisting and no temporal population subdivision (ΦPT = 0.021 & -0.003) found over three years. Collections from circular plots showed no statistical correlation between related Pocillopora individuals and their associations with particular S. glynni genotypes, with no spatial structuring or clonal aggregation across a reef for the symbiont. From permanent linear transects, samples were analyzed from multiple locations within a colony and some were re-sampled ~1 year later. Many colonies of Pocillopora (~ 53%) were dominated by a single S. glynni genotype and tended to associate with the same symbiont genotype(s) temporally, while colony ramets often possessed unrelated symbiont genotypes. The lack of correlation between host and symbiont lineages and the possibility for temporal turnover of symbiont genotypes suggests that these genotypic combinations are potentially highly flexible. Expanding to S. glynni populations distributed throughout the Eastern Pacific, a total of four hundred and two multilocus haploid genotypes were acquired, of which two hundred and fifteen were distinct. Clone, or strain, diversity was high at most collection sites, with a iii single genotype detected in most samples (> 80%). Minimal population subdivision was detected throughout the Eastern Tropical Pacific (ETP) encompassing 1000’s of square kilometers from mainland Mexico and Clipperton Atoll to the Gulf of Panama and the Galapagos Islands. The general lack of population differentiation over these distances appears to correspond with recent findings of extensive host genetic connectivity and indicates Pocillopora larvae, which maternally inherit their symbionts, aid in the dispersal of this symbiont. Unlike a confluent host population, high latitude populations in the subtropical Gulf of California (Sea of Cortez) were strongly differentiated from the ETP. The tropical (ETP) and subtropical (Gulf California, GoC) Eastern Pacific populations of S. glynni were compared to Palau in the west Pacific, and the Gulf of Thailand the Indo-Pacific. Bayesian clustering resolved several distinct populations (ΦRT = 0.280, p = 0.0001) including the previously described latitudinal separation between the GoC and ETP, which were well differentiated from populations in the west Indo-Pacific region. Additional structuring between Palau, the Gulf of Thailand and the Andaman Sea was statistically significant (ΦPR = 0.179, p = 0.0001). Latitudinal environments and large oceanic expanses appear to have structured S. glynni into genetically differentiated populations. However, several genotypes from Palau were similar in allelic composition to genotypes found in the GoC, suggesting that occasional dispersal may occur between east and west Pacific regions. While S. glynni associates with Pocillopora type 1 across the GoC and ETP, it associates with a different species of Pocillopora (genetically-defined as type 5) in western regions and this may in part explain the longitudinal differentiation. Contrasting the host specificity and vertical transmission of S. glynni, Symbiodinium trenchi (D1a) is a host generalist and horizontally transmitted. This symbiont differs ecologically from other genetically defined types within Clade D in that it is the most geographically widespread, associates with a diversity of host taxa and in the Caribbean S. trenchi has increased in prevalence and abundance in coral communities under prolonged exposure to raised sea surface temperatures. The unique ecology and distribution of this symbiont prompted an investigation into its genotypic diversity and population structuring in representative reefs from the Indo-Pacific and throughout the Atlantic using twelve diallelic microsatellite loci. Populations of S. trenchi from the Indo-Pacific were genetically diverse (I > 1.14) with most genotypes the products of sexual recombination (R > 0.80). In contrast, populations throughout the greater Caribbean were limited in genetic diversity (I = 0.67) and excessively clonal (R = 0.28). While no multilocus genotypes (MLGs) were shared among reefs in the Indo-Pacific, one unusual MLG was found forty-four times in the Caribbean and from every sample location except the Flower Garden Banks. Genotypic diversity is typically high among other Caribbean Symbiodinium spp. suggesting something is unusual about the population dynamics and dispersal of S. trenchi in this region. Severe thermal anomalies including recent events in 2005 and 2009 possibly facilitated expansion of a particularly aggressive clone lineage and/or populations of this symbiont, which may stem from a small number of opportunistic introductions originating from the Indo-Pacific. Data such as these on the population structure, genetic diversity and stability of coral/algal symbioses are necessary for inferring the processes by which these symbioses evolve and respond to changes in environmental conditions. Most symbiont populations are comprised of genotypically diverse and divergent individuals, with some symbiont genotypes found numerous times on a reef and as a result of asexual reproduction. The one extreme exception was the Caribbean S. trenchi population, which contained low allelic diversity and iv is dominated by a single MLG or symbiont clone. The stability of a population’s genotypic diversity appears stable and the dispersal of this diversity controlled by environmental conditions and oceanic currents. While both symbiont species show the propensity for long- distance dispersal, it is believed that co-dispersing with its Pocillopora host larvae enhances S. glynni’s dispersal, while S. trenchi must rely on its own intrinsic dispersal ability. Lastly, comparisons between the genetic identity of Pocillopora and S. glynni demonstrate flexibility at the individual and population level. Although these symbionts are vertically transmitted, the symbiosis is not fixed and individual associations can change in response to environmental conditions and chance events, providing the mechanism for symbiosis evolution. These findings highlight the complex nature and the species-specific patterns of population structuring and dispersal for coral-algal symbioses. v TABLE OF CONTENTS List of Tables ..........................................................................................................................vii
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