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Polymorphism in the symmetries of gastric pouch arrangements in the sea anemone D. lineata.

ABSTRACT: Symmetry in the arrangement of body parts is a distinctive phylogenetic feature of animals. Cnidarians show both bilateral and radial symmetries in their internal organs, such as gastric pouches and muscles. However, how different symmetries appear during the developmental process remains unknown. Here, we report intraspecific variations in the symmetric arrangement of gastric pouches, muscles, and siphonoglyphs, the Anthozoan-specific organ that drives water into the organism, in D. lineata (Diadumenidae, Actiniaria). We found that the positional arrangement of the internal organs was apparently constrained to either biradial or bilateral symmetries depending on the number of siphonoglyphs. Based on the morphological observations, a mathematical model of internal organ positioning was employed to predict the developmental backgrounds responsible for the biradial and bilateral symmetries. In the model, we assumed that the specification of gastric pouches is orchestrated by lateral inhibition and activation, which results in different symmetries depending on the number of siphonoglyphs. Thus, we propose that a common developmental program can generate either bilateral or biradial symmetries depending on the number of siphonoglyphs formed in the early developmental stages.

SUBMITTER: Sarper SE

PROVIDER: S-EPMC8419960 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:The lined sea anemone Edwardsiella lineata is an informative model system for evolutionary-developmental studies of parasitism. In this species, it is possible to compare alternate developmental pathways leading from a larva to either a free-living polyp or a vermiform parasite that inhabits the mesoglea of a ctenophore host. Additionally, E. lineata is confamilial with the model cnidarian Nematostella vectensis, providing an opportunity for comparative genomic, molecular and organismal studies. DESCRIPTION:We generated a reference transcriptome for E. lineata via high-throughput sequencing of RNA isolated from five developmental stages (parasite; parasite-to-larva transition; larva; larva-to-adult transition; adult). The transcriptome comprises 90,440 contigs assembled from >15 billion nucleotides of DNA sequence. Using a molecular clock approach, we estimated the divergence between E. lineata and N. vectensis at 215-364 million years ago. Based on gene ontology and metabolic pathway analyses and gene family surveys (bHLH-PAS, deiodinases, Fox genes, LIM homeodomains, minicollagens, nuclear receptors, Sox genes, and Wnts), the transcriptome of E. lineata is comparable in depth and completeness to N. vectensis. Analyses of protein motifs and revealed extensive conservation between the proteins of these two edwardsiid anemones, although we show the NF-?B protein of E. lineata reflects the ancestral structure, while the NF-?B protein of N. vectensis has undergone a split that separates the DNA-binding domain from the inhibitory domain. All contigs have been deposited in a public database (EdwardsiellaBase), where they may be searched according to contig ID, gene ontology, protein family motif (Pfam), enzyme commission number, and BLAST. The alignment of the raw reads to the contigs can also be visualized via JBrowse. CONCLUSIONS:The transcriptomic data and database described here provide a platform for studying the evolutionary developmental genomics of a derived parasitic life cycle. In addition, these data from E. lineata will aid in the interpretation of evolutionary novelties in gene sequence or structure that have been reported for the model cnidarian N. vectensis (e.g., the split NF-?B locus). Finally, we include custom computational tools to facilitate the annotation of a transcriptome based on high-throughput sequencing data obtained from a "non-model system."

Project description: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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Polymorphism in the symmetries of gastric pouch arrangements in the sea anemone D. lineata.

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