Dataset Information

Mitochondrial DNA hyperdiversity and its potential causes in the marine periwinkle Melarhaphe neritoides (Mollusca: Gastropoda).

ABSTRACT: We report the presence of mitochondrial DNA (mtDNA) hyperdiversity in the marine periwinkle Melarhaphe neritoides (Linnaeus, 1758), the first such case among marine gastropods. Our dataset consisted of concatenated 16S-COI-Cytb gene fragments. We used Bayesian analyses to investigate three putative causes underlying genetic variation, and estimated the mtDNA mutation rate, possible signatures of selection and the effective population size of the species in the Azores archipelago. The mtDNA hyperdiversity in M. neritoides is characterized by extremely high haplotype diversity (Hd = 0.999 ± 0.001), high nucleotide diversity (? = 0.013 ± 0.001), and neutral nucleotide diversity above the threshold of 5% (?_syn = 0.0677). Haplotype richness is very high even at spatial scales as small as 100m². Yet, mtDNA hyperdiversity does not affect the ability of DNA barcoding to identify M. neritoides. The mtDNA hyperdiversity in M. neritoides is best explained by the remarkably high mutation rate at the COI locus (? = 5.82 × 10^-5 per site per year or ? = 1.99 × 10^-4 mutations per nucleotide site per generation), whereas the effective population size of this planktonic-dispersing species is surprisingly small (N_e = 5, 256; CI = 1,312-3,7495) probably due to the putative influence of selection. Comparison with COI nucleotide diversity values in other organisms suggests that mtDNA hyperdiversity may be more frequently linked to high ? values and that mtDNA hyperdiversity may be more common across other phyla than currently appreciated.

SUBMITTER: Fourdrilis S

PROVIDER: S-EPMC5068447 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Publications

Mitochondrial DNA hyperdiversity and its potential causes in the marine periwinkle Melarhaphe neritoides (Mollusca: Gastropoda).

Fourdrilis Séverine S Mardulyn Patrick P Hardy Olivier J OJ Jordaens Kurt K de Frias Martins António Manuel AM Backeljau Thierry T

PeerJ 20161005

We report the presence of mitochondrial DNA (mtDNA) hyperdiversity in the marine periwinkle Melarhaphe neritoides (Linnaeus, 1758), the first such case among marine gastropods. Our dataset consisted of concatenated 16S-COI-Cytb gene fragments. We used Bayesian analyses to investigate three putative causes underlying genetic variation, and estimated the mtDNA mutation rate, possible signatures of selection and the effective population size of the species in the Azores archipelago. T ...[more]

PMID: 27761337

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Project description:BACKGROUND: Reconstructing the higher relationships of pulmonate gastropods has been difficult. The use of morphology is problematic due to high homoplasy. Molecular studies have suffered from low taxon sampling. Forty-eight complete mitochondrial genomes are available for gastropods, ten of which are pulmonates. Here are presented the new complete mitochondrial genomes of the ten following species of pulmonates: Salinator rhamphidia (Amphiboloidea); Auriculinella bidentata, Myosotella myosotis, Ovatella vulcani, and Pedipes pedipes (Ellobiidae); Peronia peronii (Onchidiidae); Siphonaria gigas (Siphonariidae); Succinea putris (Stylommatophora); Trimusculus reticulatus (Trimusculidae); and Rhopalocaulis grandidieri (Veronicellidae). Also, 94 new pulmonate-specific primers across the entire mitochondrial genome are provided, which were designed for amplifying entire mitochondrial genomes through short reactions and closing gaps after shotgun sequencing. RESULTS: The structural features of the 10 new mitochondrial genomes are provided. All genomes share similar gene orders. Phylogenetic analyses were performed including the 10 new genomes and 17 genomes from Genbank (outgroups, opisthobranchs, and other pulmonates). Bayesian Inference and Maximum Likelihood analyses, based on the concatenated amino-acid sequences of the 13 protein-coding genes, produced the same topology. The pulmonates are paraphyletic and basal to the opisthobranchs that are monophyletic at the tip of the tree. Siphonaria, traditionally regarded as a basal pulmonate, is nested within opisthobranchs. Pyramidella, traditionally regarded as a basal (non-euthyneuran) heterobranch, is nested within pulmonates. Several hypotheses are rejected, such as the Systellommatophora, Geophila, and Eupulmonata. The Ellobiidae is polyphyletic, but the false limpet Trimusculus reticulatus is closely related to some ellobiids. CONCLUSIONS: Despite recent efforts for increasing the taxon sampling in euthyneuran (opisthobranchs and pulmonates) molecular phylogenies, several of the deeper nodes are still uncertain, because of low support values as well as some incongruence between analyses based on complete mitochondrial genomes and those based on individual genes (18S, 28S, 16S, CO1). Additional complete genomes are needed for pulmonates (especially for Williamia, Otina, and Smeagol), as well as basal heterobranchs closely related to euthyneurans. Increasing the number of markers for gastropod (and more broadly mollusk) phylogenetics also is necessary in order to resolve some of the deeper nodes -although clearly not an easy task. Step by step, however, new relationships are being unveiled, such as the close relationships between the false limpet Trimusculus and ellobiids, the nesting of pyramidelloids within pulmonates, and the close relationships of Siphonaria to sacoglossan opisthobranchs. The additional genomes presented here show that some species share an identical mitochondrial gene order due to convergence.

Dataset Information

Mitochondrial DNA hyperdiversity and its potential causes in the marine periwinkle Melarhaphe neritoides (Mollusca: Gastropoda).

Publications

Mitochondrial DNA hyperdiversity and its potential causes in the marine periwinkle <i>Melarhaphe neritoides</i> (Mollusca: Gastropoda).

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