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Ten new complete mitochondrial genomes of pulmonates (Mollusca: Gastropoda) and their impact on phylogenetic relationships.

White TR, Conrad MM, Tseng R, Balayan S, Golding R, de Frias Martins AM, Dayrat BA - BMC Evol. Biol. (2011)

Bottom Line: Additional complete genomes are needed for pulmonates (especially for Williamia, Otina, and Smeagol), as well as basal heterobranchs closely related to euthyneurans.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: School of Natural Sciences, University of California, 5200 North Lake Road, Merced, CA 95343, USA.

ABSTRACT

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.

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Hypothesized gene rearrangements of the genomes included in the present study. The phylogenetic topology is from the present study. Genes encoded by the minus strand are underlined.
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Figure 4: Hypothesized gene rearrangements of the genomes included in the present study. The phylogenetic topology is from the present study. Genes encoded by the minus strand are underlined.

Mentions: Biomphalaria glabrata, Salinator rhamphidia, Trimusculus reticulatus, Ovatella vulcani, Auriculinella bidentata, Peronia peronii, Onchidella borealis, Onchidella celtica share an identical mitochondrial genome organization (Figure 4). Albinaria coerulea shares the same genome organization except that the position of trnS1 and trnS2 are switched and trnS1 is inverted. The genome of the two freshwater snails Radix balthica and Biomphalaria glabrata differ in the location of five tRNAs (P, H, G, C, and Y). The genome of Rhopalocaulis grandidieri differs in the location of seven tRNAs (C, F, G, W, H, L2, and E). The genome of Succinea putris differs in the location of three tRNAs (F, Y, and W), with the latter two genes being coded on the minus strand instead of the plus strand. In Pedipes pedipes, trnT, cox3 swapped with trnS1, nad4, and trnQ and trnR moved between these two swapped sets of genes. Myosotella myosotis only differs from the most standard mitochondrial genome organization by the rearrangement of nad4L between cox2 and trnY. The location of trnY before cox1 is a unique and unusual feature of the mitochondrial genome of Pyramidella dolabrata. Other attributes, such as the location of atp6 prior to atp8 and the encoding of trnG by the minus strand, are exclusive to Pyramidella dolabrata.


Ten new complete mitochondrial genomes of pulmonates (Mollusca: Gastropoda) and their impact on phylogenetic relationships.

White TR, Conrad MM, Tseng R, Balayan S, Golding R, de Frias Martins AM, Dayrat BA - BMC Evol. Biol. (2011)

Hypothesized gene rearrangements of the genomes included in the present study. The phylogenetic topology is from the present study. Genes encoded by the minus strand are underlined.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3198971&req=5

Figure 4: Hypothesized gene rearrangements of the genomes included in the present study. The phylogenetic topology is from the present study. Genes encoded by the minus strand are underlined.
Mentions: Biomphalaria glabrata, Salinator rhamphidia, Trimusculus reticulatus, Ovatella vulcani, Auriculinella bidentata, Peronia peronii, Onchidella borealis, Onchidella celtica share an identical mitochondrial genome organization (Figure 4). Albinaria coerulea shares the same genome organization except that the position of trnS1 and trnS2 are switched and trnS1 is inverted. The genome of the two freshwater snails Radix balthica and Biomphalaria glabrata differ in the location of five tRNAs (P, H, G, C, and Y). The genome of Rhopalocaulis grandidieri differs in the location of seven tRNAs (C, F, G, W, H, L2, and E). The genome of Succinea putris differs in the location of three tRNAs (F, Y, and W), with the latter two genes being coded on the minus strand instead of the plus strand. In Pedipes pedipes, trnT, cox3 swapped with trnS1, nad4, and trnQ and trnR moved between these two swapped sets of genes. Myosotella myosotis only differs from the most standard mitochondrial genome organization by the rearrangement of nad4L between cox2 and trnY. The location of trnY before cox1 is a unique and unusual feature of the mitochondrial genome of Pyramidella dolabrata. Other attributes, such as the location of atp6 prior to atp8 and the encoding of trnG by the minus strand, are exclusive to Pyramidella dolabrata.

Bottom Line: Additional complete genomes are needed for pulmonates (especially for Williamia, Otina, and Smeagol), as well as basal heterobranchs closely related to euthyneurans.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: School of Natural Sciences, University of California, 5200 North Lake Road, Merced, CA 95343, USA.

ABSTRACT

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.

Show MeSH
Related in: MedlinePlus