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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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List of complete gastropod mitochondrial genomes available at present. The hypothesis of phylogenetic relationships is based on both morphological and molecular data [46]. The reference in which each genome was made available [6-11,47-58] is indicated in brackets as well as the year of publication.
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Figure 2: List of complete gastropod mitochondrial genomes available at present. The hypothesis of phylogenetic relationships is based on both morphological and molecular data [46]. The reference in which each genome was made available [6-11,47-58] is indicated in brackets as well as the year of publication.

Mentions: Analyses based on complete mitochondrial genomes provide different phylogenetic relationships, at least for the deep nodes [6-8]: pulmonates are paraphyletic, basal to the monophyletic opisthobranchs; Siphonaria is nested within the opisthobranchs. Taxon sampling is still limited in analyses based on complete mitochondrial genomes, mainly because gastropod mitochondrial genomes are still difficult to obtain. Since the first complete gastropod mitochondrial genome was published in 1995 [9], 48 complete genomes have been made available (Figure 2). The use of shotgun sequencing and the decrease in sequencing costs caused a noticeable increase in the production of gastropod mitochondrial genomes a few years ago (Figure 2). Ten genomes became available in nine different publications between 1995 and 2006; since 2008, 38 genomes became available, 30 of which appeared in only four publications [6,8,10,11], although a few papers with only one genome were also published.


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)

List of complete gastropod mitochondrial genomes available at present. The hypothesis of phylogenetic relationships is based on both morphological and molecular data [46]. The reference in which each genome was made available [6-11,47-58] is indicated in brackets as well as the year of publication.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: List of complete gastropod mitochondrial genomes available at present. The hypothesis of phylogenetic relationships is based on both morphological and molecular data [46]. The reference in which each genome was made available [6-11,47-58] is indicated in brackets as well as the year of publication.
Mentions: Analyses based on complete mitochondrial genomes provide different phylogenetic relationships, at least for the deep nodes [6-8]: pulmonates are paraphyletic, basal to the monophyletic opisthobranchs; Siphonaria is nested within the opisthobranchs. Taxon sampling is still limited in analyses based on complete mitochondrial genomes, mainly because gastropod mitochondrial genomes are still difficult to obtain. Since the first complete gastropod mitochondrial genome was published in 1995 [9], 48 complete genomes have been made available (Figure 2). The use of shotgun sequencing and the decrease in sequencing costs caused a noticeable increase in the production of gastropod mitochondrial genomes a few years ago (Figure 2). Ten genomes became available in nine different publications between 1995 and 2006; since 2008, 38 genomes became available, 30 of which appeared in only four publications [6,8,10,11], although a few papers with only one genome were also published.

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