Genome-wide polymorphism and signatures of selection in the symbiotic sea anemone Aiptasia

BMC Genomics, Feb 2016

Background Coral reef ecosystems are declining in response to global climate change and anthropogenic impacts. Yet patterns of standing genetic variation within cnidarian species, a major determinant of adaptive potential, are virtually unknown at genome-scale resolution. We explore patterns of genome-wide polymorphism and identify candidate loci under selection in the sea anemone Aiptasia, an important laboratory model system for studying the symbiosis between corals and dinoflagellate algae of the genus Symbiodinium. Results Low coverage genome sequencing revealed large genetic distances among globally widespread lineages, novel candidate targets of selection, and considerably higher heterozygosity than previously reported for Aiptasia. More than 670,000 single nucleotide polymorphisms were identified among 10 Aiptasia individuals including two pairs of genetic clones. Evolutionary relationships based on genome-wide polymorphism supported the current paradigm of a genetically distinct population from the US South Atlantic that harbors diverse Symbiodinium clades. However, anemones from the US South Atlantic demonstrated a striking lack of shared derived polymorphism. Heterozygosity was an important feature shaping nucleotide diversity patterns: at any given SNP site, more than a third of individuals genotyped were heterozygotes, and heterozygosity within individual genomes ranged from 0.37–0.58 %. Analysis of nonsynonymous and synonymous sites suggested that highly heterozygous regions are evolving under relaxed purifying selection compared to the rest of the Aiptasia genome. Genes previously identified as having elevated evolutionary rates in Aiptasia compared to other cnidarians were found in our study to be under strong purifying selection within Aiptasia. Candidate targets of selection, including lectins and genes involved in Rho GTPase signalling, were identified based on unusual signatures of nucleotide diversity, Tajima’s D, and heterozygosity compared to genome-wide averages. Conclusions This study represents the first genome-wide analysis of Tajima’s D in a cnidarian. Our results shed light on patterns of intraspecific genome-wide polymorphism in a model for studies of coral-algae symbiosis and present genetic targets for future research on evolutionary and cellular processes in early-diverging metazoans.

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Genome-wide polymorphism and signatures of selection in the symbiotic sea anemone Aiptasia

Bellis et al. BMC Genomics Genome-wide polymorphism and signatures of selection in the symbiotic sea anemone Aiptasia Emily S. Bellis 0 Dana K. Howe 0 Dee R. Denver 0 0 Department of Integrative Biology, Oregon State University , Corvallis 97331OR , USA Background: Coral reef ecosystems are declining in response to global climate change and anthropogenic impacts. Yet patterns of standing genetic variation within cnidarian species, a major determinant of adaptive potential, are virtually unknown at genome-scale resolution. We explore patterns of genome-wide polymorphism and identify candidate loci under selection in the sea anemone Aiptasia, an important laboratory model system for studying the symbiosis between corals and dinoflagellate algae of the genus Symbiodinium. Results: Low coverage genome sequencing revealed large genetic distances among globally widespread lineages, novel candidate targets of selection, and considerably higher heterozygosity than previously reported for Aiptasia. More than 670,000 single nucleotide polymorphisms were identified among 10 Aiptasia individuals including two pairs of genetic clones. Evolutionary relationships based on genome-wide polymorphism supported the current paradigm of a genetically distinct population from the US South Atlantic that harbors diverse Symbiodinium clades. However, anemones from the US South Atlantic demonstrated a striking lack of shared derived polymorphism. Heterozygosity was an important feature shaping nucleotide diversity patterns: at any given SNP site, more than a third of individuals genotyped were heterozygotes, and heterozygosity within individual genomes ranged from 0.37-0.58 %. Analysis of nonsynonymous and synonymous sites suggested that highly heterozygous regions are evolving under relaxed purifying selection compared to the rest of the Aiptasia genome. Genes previously identified as having elevated evolutionary rates in Aiptasia compared to other cnidarians were found in our study to be under strong purifying selection within Aiptasia. Candidate targets of selection, including lectins and genes involved in Rho GTPase signalling, were identified based on unusual signatures of nucleotide diversity, Tajima's D, and heterozygosity compared to genome-wide averages. Conclusions: This study represents the first genome-wide analysis of Tajima's D in a cnidarian. Our results shed light on patterns of intraspecific genome-wide polymorphism in a model for studies of coral-algae symbiosis and present genetic targets for future research on evolutionary and cellular processes in early-diverging metazoans. Cnidarian symbiosis; heterozygosity; Tajima's D; genome skimming; Symbiodinium Background Intimate mutualistic associations between photosynthetic algae and invertebrates are integral to the ecology of marine environments. Perhaps the most well-studied invertebrate-algal symbiosis is that between reef-building corals and unicellular photosynthetic algae of the genus Symbiodinium, though endosymbioses with Symbiodinium are pervasive throughout the phylum Cnidaria, which includes corals, jellyfish, and sea anemones. In these nutritional symbioses, algal symbionts reside inside cells of the cnidarian gastroderm, where they can access CO2 and other host metabolic byproducts containing nitrogen and phosphorus (reviewed in [ 1 ]). In return, the cnidarian host receives compounds derived from algal photosynthesis that support host growth, reproduction, and metabolism [ 2 ]. The impact of this relationship extends beyond the cnidarian host and algal symbiont to influence the tremendous biodiversity harbored by coral reefs, the cycling of nutrients in oligotrophic marine environments, and fisheries and tourism-based economies that depend on healthy reef ecosystems. Rising ocean temperatures disrupt invertebrate-algal symbioses, causing expulsion of symbiotic algae from cnidarian host tissues, or “bleaching” [ 3, 4 ]. Yet, the processes through which corals might respond to ocean warming in the long-term remain unclear [5]. Potential responses range from short-term physiological changes to those occurring on evolutionary timescales. Physiological acclimation has been increasingly shown to play a crucial role in the thermal tolerance of corals [ 6, 7 ]. Others have suggested that corals may respond to elevated temperatures on rapid timescales by harboring more thermally resistant Symbiodinium communities, either increasing abundance of background genotypes or establishing symbioses with new symbiont genotypes altogether [ 8–10 ]. Characterized by expansive, uniquely structured genomes of ~1.5–5 Gbp [ 11, 12 ], Symbiodinium are a hyperdiverse genus organized into nine distinct subgeneric clades (clades A-I) [ 13, 14 ]. Decreased bleaching has been demonstrated in corals following shifts to putatively more thermotolerant clade D Symbiodinium communities [ 10, 15 ], but symbiotic associations with more thermotolerant partners may be s (...truncated)


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Emily Bellis, Dana Howe, Dee Denver. Genome-wide polymorphism and signatures of selection in the symbiotic sea anemone Aiptasia, BMC Genomics, 2016, pp. 160, 17, DOI: 10.1186/s12864-016-2488-6