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

Fourdrilis, Séverine; Mardulyn, Patrick; Hardy, Olivier J.; Jordaens, Kurt; Martins, António M. de Frias; Backeljau, Thierry

doi:10.7717/peerj.2549

Cited by 18 publications

(26 citation statements)

References 136 publications

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“…High levels of mitochondrial polymorphism among individuals of L. bulimoides could have further complicated the capture, resulting in low capture success of mitochondrial targets. Hyperdiversity in mitochondrial genes, with more than 5% nucleotide diversity in synonymous sites has been reported for several animal clades, including gastropods [63,64] and chaetognaths [65]. Only 13 of the 41 non-coding targeted regions were recovered, which may indicate that these regions were also too divergent to be captured by the probes.…”

Section: Target Capture Probes For Limacina Bulimoidesmentioning

confidence: 96%

Novel genomic resources for shelled pteropods: a draft genome and target capture probes for Limacina bulimoides, tested for cross-species relevance

et al. 2020

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Background: Pteropods are planktonic gastropods that are considered as bio-indicators to monitor impacts of ocean acidification on marine ecosystems. In order to gain insight into their adaptive potential to future environmental changes, it is critical to use adequate molecular tools to delimit species and population boundaries and to assess their genetic connectivity. We developed a set of target capture probes to investigate genetic variation across their large-sized genome using a population genomics approach. Target capture is less limited by DNA amount and quality than other genome-reduced representation protocols, and has the potential for application on closely related species based on probes designed from one species. Results: We generated the first draft genome of a pteropod, Limacina bulimoides, resulting in a fragmented assembly of 2.9 Gbp. Using this assembly and a transcriptome as a reference, we designed a set of 2899 genomewide target capture probes for L. bulimoides. The set of probes includes 2812 single copy nuclear targets, the 28S rDNA sequence, ten mitochondrial genes, 35 candidate biomineralisation genes, and 41 non-coding regions. The capture reaction performed with these probes was highly efficient with 97% of the targets recovered on the focal species. A total of 137,938 single nucleotide polymorphism markers were obtained from the captured sequences across a test panel of nine individuals. The probes set was also tested on four related species: L. trochiformis, L. lesueurii, L. helicina, and Heliconoides inflatus, showing an exponential decrease in capture efficiency with increased genetic distance from the focal species. Sixty-two targets were sufficiently conserved to be recovered consistently across all five species. Conclusion: The target capture protocol used in this study was effective in capturing genome-wide variation in the focal species L. bulimoides, suitable for population genomic analyses, while providing insights into conserved genomic regions in related species. The present study provides new genomic resources for pteropods and supports the use of target capture-based protocols to efficiently characterise genomic variation in small non-model organisms with large genomes.

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Section: Target Capture Probes For Limacina Bulimoidesmentioning

confidence: 96%

Novel genomic resources for shelled pteropods: a draft genome and target capture probes for Limacina bulimoides, tested for cross-species relevance

et al. 2020

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“…its selectively neutral nucleotide diversity is above the threshold of 5% (see 1 for this definition and threshold), for the cytochrome oxidase c subunit I ( cox1 ) and cytochrome b ( cob ) genes ( π syn = 7.4 and 6.4% respectively). This is probably due to an extremely high mtDNA mutation rate ( µ = 5.82 × 10 −5 per site per year at the cox1 locus) 2 . Across eukaryotic phyla, such mtDNA hyperdiversity may be more common than currently appreciated 2 .…”

Section: Introductionmentioning

confidence: 99%

“…This is probably due to an extremely high mtDNA mutation rate ( µ = 5.82 × 10 −5 per site per year at the cox1 locus) 2 . Across eukaryotic phyla, such mtDNA hyperdiversity may be more common than currently appreciated 2 .…”

Section: Introductionmentioning

confidence: 99%

Relation between mitochondrial DNA hyperdiversity, mutation rate and mitochondrial genome evolution in Melarhaphe neritoides (Gastropoda: Littorinidae) and other Caenogastropoda

Fourdrilis

Martins

Backeljau

2018

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Mitochondrial DNA hyperdiversity is primarily caused by high mutation rates (µ) and has potential implications for mitogenome architecture and evolution. In the hyperdiverse mtDNA of Melarhaphe neritoides (Gastropoda: Littorinidae), high mutational pressure generates unusually large amounts of synonymous variation, which is expected to (1) promote changes in synonymous codon usage, (2) reflect selection at synonymous sites, (3) increase mtDNA recombination and gene rearrangement, and (4) be correlated with high mtDNA substitution rates. The mitogenome of M. neritoides was sequenced, compared to closely related littorinids and put in the phylogenetic context of Caenogastropoda, to assess the influence of mtDNA hyperdiversity and high µ on gene content and gene order. Most mitogenome features are in line with the trend in Mollusca, except for the atypical secondary structure of the methionine transfer RNA lacking the TΨC-loop. Therefore, mtDNA hyperdiversity and high µ in M. neritoides do not seem to affect its mitogenome architecture. Synonymous sites are under positive selection, which adds to the growing evidence of non-neutral evolution at synonymous sites. Under such non-neutrality, substitution rate involves neutral and non-neutral substitutions, and high µ is not necessarily associated with high substitution rate, thus explaining that, unlike high µ, a high substitution rate is associated with gene order rearrangement.

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“…The sampling size did not capture the entire genetic diversity of the species as shown by the rarefaction curve, and did not provide a reasonable number of shared haplotypes. Moreover, abnormally high mutation rates may obscure the signal of gene flow 49 . The haplotype network (Fig.…”

Section: Hyperdiversity In Diplodus Bellottiimentioning

confidence: 99%

“…This mitochondrial region is a marker of choice in phylogeographic and connectivity studies (but on the use of hyperdiverse mtDNA for population differentiation see 46 ). The gastropod Melarhaphe neritoides revealed hypervariable mitochondrial DNA markers (16S, COI and Cytb) as a consequence of high mutation rates 49 . The second hypothesis used to explain high mutation rates in tropical areas (D. bellottii is considered a subtropical fish species), suggests that temperature and UV tend to generally increase mutation rates in the mtDNA of vertebrates 52 .…”

Section: Hyperdiversity In Diplodus Bellottiimentioning

confidence: 99%

Against all odds: a tale of marine range expansion with maintenance of extremely high genetic diversity

Robalo

Francisco

Vendrell

et al. 2020

Sci Rep

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the displacement of species from equatorial latitudes to temperate locations following the increase in sea surface temperatures is among the significant reported consequences of climate change. Shifts in the distributional ranges of species result in fish communities tropicalisation, i.e., high latitude colonisations by typically low latitude distribution species. these movements create new interactions between species and new trophic assemblages. the Senegal seabream, Diplodus bellottii, may be used as a model to understand the population genetics of these invasions. in the last decades, this species has undergone an outstanding range expansion from its African area of origin to the Atlantic coast of the iberian peninsula, where now occurs abundantly. Mitochondrial and nuclear markers revealed a striking high haplotypic nucleotide and genetic diversity values, along with significant population differentiation throughout the present-day geographical range of the Senegal seabream. These results are not consistent with the central-marginal hypothesis, nor with the expectations of a leptokurtic distribution of individuals, as D. bellottii seems to be able to retain exceptional levels of diversity in marginal and recently colonised areas. We discuss possible causes for hyperdiversity and lack of geographical structure and subsequent implications for fisheries. Tropicalisation, the displacement of species from equatorial latitudes to temperate locations, is one of the major reported consequences of climate changes 1-3. The increase of sea surface temperatures (SSTs) in the last decades has promoted shifts in the distributional ranges of species (e.g., 4,5) with individuals moving into areas best corresponding to their physiological optimum. Additionally, the ability of a species to colonise new habitats is influenced by oceanographic currents, the existence of adequate resource availability (i.e., habitat and food) and life-history patterns (e.g., number of eggs produced, age or parental care). These movements lead to the colonization of more poleward habitats by low latitude species, and create new interactions between species and new trophic assemblages. In commercial species, these shifts due to climate change can be magnified by fishing pressures, as reported for the North Sea cod (e.g., 6). Poleward colonization by organisms with a typically equatorial distribution was described almost three decades ago for terrestrial organisms in association with postglacial recolonisation routes (e.g., 7-10). As a general rule, organisms follow a leptokurtic distribution type, in which the majority of individuals stay at or near the original area, and only a fraction disperse to longer distances. This range extension is usually done in a steppingstone manner, implying that each settlement has fewer individuals compared with the previous one. Theoretically, this process corresponds to multiple successive genetic founder events associated with the corresponding genetic implications of the downsize in the effective population num...

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

Cited by 18 publications

References 136 publications

Novel genomic resources for shelled pteropods: a draft genome and target capture probes for Limacina bulimoides, tested for cross-species relevance

Novel genomic resources for shelled pteropods: a draft genome and target capture probes for Limacina bulimoides, tested for cross-species relevance

Relation between mitochondrial DNA hyperdiversity, mutation rate and mitochondrial genome evolution in Melarhaphe neritoides (Gastropoda: Littorinidae) and other Caenogastropoda

Against all odds: a tale of marine range expansion with maintenance of extremely high genetic diversity

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