Abstract

BackgroundCoral 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.ResultsLow 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.ConclusionsThis 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2488-6) contains supplementary material, which is available to authorized users.

Highlights

  • Coral reef ecosystems are declining in response to global climate change and anthropogenic impacts

  • The proportions of mapped reads from BM1 and HI1 were within the range of values for the symbiotic samples, suggesting a relatively low contribution of Symbiodinium sequences to the genomic libraries

  • An improved basic understanding of evolutionary processes and population-genomic structuring is crucial to predicting responses of symbiotic cnidarians, including reef-building corals, to rapid climate change [23, 67]

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Summary

Introduction

Coral reef ecosystems are declining in response to global climate change and anthropogenic impacts. 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]). 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. The diversity of cnidarian-Symbiodinium associations regionally, temporally, and even spatially across areas of a single colony underscores the complex nature of cnidarian responses to changing environments [19,20,21]

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