Evolutionary Insights into Cnidarian-Dinoflagellate Symbiosis from Natural Variation in Aiptasia Sea Anemones Public Deposited

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  • Mutualistic associations between corals and symbiotic microalgae of the genus Symbiodium power tropical reef ecosystems, hotspots of marine biodiversity that buffer coastlines, support tourism- and fisheries-based economies, and offer untapped potential for discovery of novel pharmaceutical compounds. However, reef ecosystems are declining at an alarming rate, in large part due to severe episodes of coral bleaching, or breakdown of the coral-Symbiodinium symbiosis. The sea anemone Aiptasia has emerged as a laboratory model system for understanding coral-Symbiodinium interactions at multiple biological levels. To further develop Aiptasia as an evolutionary model system, the goal of my dissertation work was to characterize natural variation in Aiptasia-Symbiodinium symbioses by (1) examining genome-wide polymorphism among global anemone lineages, (2) experimentally evaluating natural variation in bleaching response, and (3) investigating patterns of genetic variation in natural populations across diverse abiotic environments. In Chapter 2, I use low-coverage genome skimming to investigate polymorphism in well-studied laboratory strains hosting diverse Symbiodinium, revealing that higher genetic diversity exists in Aiptasia from the Western Atlantic compared to a more globally distributed lineage. I further compare polymorphisms in sliding windows across the genome to identify candidate genes under balancing and positive selection based on patterns of heterozygosity, nucleotide diversity, and Tajima’s D. In Chapter 3, I characterize bleaching of Aiptasia lab strains to different stressors and discover significant variation in responses to acute heat stress but not to cold-shock. In Chapter 4, I examine potential relationships between abiotic environmental variation and genetic variation of anemone-Symbiodinium assemblages in the wild, at four locations in Caribbean Panama where long-term environmental datasets are available. High-throughput genotyping of anemone populations revealed the presence of a closely related cryptic species, Exaiptasia brasiliensis, and striking differences in anemone abundance, distribution, and patterns of symbiont association across environments. An Aiptasia sub-population specific to the Bocas del Toro Archipelago is described, with strong differentiation compared to the global population at several loci predicted to be important for mediating interactions with Symbiodinium. Analyses further suggest that the spatial extent of clonal reproduction in natural populations could be somewhat limited. Overall, Chapters 2-4 support a widespread global Aiptasia population distributed throughout tropical and subtropical latitudes with one or more diverged lineages, diversity of both host lineages and holobiont assemblages centered in the tropical Western Atlantic, and holobiont distribution patterns that may be strongly influenced by abiotic environment. Future studies leveraging natural variation in the Aiptasia model system described here hold great promise for advancing our fundamental knowledge of the evolution of symbiotic interactions in the sea.
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