Monoplacophoran mitochondrial genomes: convergent gene arrangements and little phylogenetic signal

Abstract Background Although recent studies have greatly advanced understanding of deep molluscan phylogeny, placement of some taxa remains uncertain as different datasets support competing class-relationships. Traditionally, morphologists have placed Monoplacophora, a group of morphologically simpl...

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Main Authors: I. Stöger, K. Kocot, A. Poustka, N. Wilson, D. Ivanov, K. Halanych, M. Schrödl
Format: Article in Journal/Newspaper
Language:unknown
Published: Figshare 2016
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Online Access:https://dx.doi.org/10.6084/m9.figshare.c.3647534.v1
https://figshare.com/collections/Monoplacophoran_mitochondrial_genomes_convergent_gene_arrangements_and_little_phylogenetic_signal/3647534/1
id ftdatacite:10.6084/m9.figshare.c.3647534.v1
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spelling ftdatacite:10.6084/m9.figshare.c.3647534.v1 2023-05-15T13:58:07+02:00 Monoplacophoran mitochondrial genomes: convergent gene arrangements and little phylogenetic signal I. Stöger K. Kocot A. Poustka N. Wilson D. Ivanov K. Halanych M. Schrödl 2016 https://dx.doi.org/10.6084/m9.figshare.c.3647534.v1 https://figshare.com/collections/Monoplacophoran_mitochondrial_genomes_convergent_gene_arrangements_and_little_phylogenetic_signal/3647534/1 unknown Figshare https://dx.doi.org/10.1186/s12862-016-0829-3 https://dx.doi.org/10.6084/m9.figshare.c.3647534 CC BY 4.0 https://creativecommons.org/licenses/by/4.0 CC-BY Cell Biology Genetics FOS Biological sciences Evolutionary Biology Ecology 69999 Biological Sciences not elsewhere classified Cancer Inorganic Chemistry FOS Chemical sciences Collection article 2016 ftdatacite https://doi.org/10.6084/m9.figshare.c.3647534.v1 https://doi.org/10.1186/s12862-016-0829-3 https://doi.org/10.6084/m9.figshare.c.3647534 2021-11-05T12:55:41Z Abstract Background Although recent studies have greatly advanced understanding of deep molluscan phylogeny, placement of some taxa remains uncertain as different datasets support competing class-relationships. Traditionally, morphologists have placed Monoplacophora, a group of morphologically simple, limpet-like molluscs as sister group to all other conchiferans (shelled molluscs other than Polyplacophora), a grouping that is supported by the latest large-scale phylogenomic study that includes Laevipilina. However, molecular datasets dominated by nuclear ribosomal genes support Monoplacophora + Polyplacophora (Serialia). Here, we evaluate the potential of mitochondrial genome data for resolving placement of Monoplacophora. Results Two complete (Laevipilina antarctica and Vema ewingi) and one partial (Laevipilina hyalina) mitochondrial genomes were sequenced, assembled, and compared. All three genomes show a highly similar architecture including an unusually high number of non-coding regions. Comparison of monoplacophoran gene order shows a gene arrangement pattern not previously reported; there is an inversion of one large gene cluster. Our reanalyses of recently published polyplacophoran mitogenomes show, however, that this feature is also present in some chiton species. Maximum Likelihood and Bayesian Inference analyses of 13 mitochondrial protein-coding genes failed to robustly place Monoplacophora and hypothesis testing could not reject any of the evaluated placements of Monoplacophora. Conclusions Under both serialian or aculiferan-conchiferan scenarios, the observed gene cluster inversion appears to be a convergent evolution of gene arrangements in molluscs. Our phylogenetic results are inconclusive and sensitive to taxon sampling. Aculifera (Polyplacophora + Aplacophora) and Conchifera were never recovered. However, some analyses recovered Serialia (Monoplacophora + Polyplacophora), Diasoma (Bivalvia + Scaphopoda) or Pleistomollusca (Bivalvia + Gastropoda). Although we could not shed light on deep evolutionary traits of Mollusca we found unique patterns of gene arrangements that are common to monoplacophoran and chitonine polyplacophoran species but not to acanthochitonine Polyplacophora. Graphical abstract Complete mitochondrial genome of Laevipilina antarctica Article in Journal/Newspaper Antarc* Antarctica DataCite Metadata Store (German National Library of Science and Technology)
institution Open Polar
collection DataCite Metadata Store (German National Library of Science and Technology)
op_collection_id ftdatacite
language unknown
topic Cell Biology
Genetics
FOS Biological sciences
Evolutionary Biology
Ecology
69999 Biological Sciences not elsewhere classified
Cancer
Inorganic Chemistry
FOS Chemical sciences
spellingShingle Cell Biology
Genetics
FOS Biological sciences
Evolutionary Biology
Ecology
69999 Biological Sciences not elsewhere classified
Cancer
Inorganic Chemistry
FOS Chemical sciences
I. Stöger
K. Kocot
A. Poustka
N. Wilson
D. Ivanov
K. Halanych
M. Schrödl
Monoplacophoran mitochondrial genomes: convergent gene arrangements and little phylogenetic signal
topic_facet Cell Biology
Genetics
FOS Biological sciences
Evolutionary Biology
Ecology
69999 Biological Sciences not elsewhere classified
Cancer
Inorganic Chemistry
FOS Chemical sciences
description Abstract Background Although recent studies have greatly advanced understanding of deep molluscan phylogeny, placement of some taxa remains uncertain as different datasets support competing class-relationships. Traditionally, morphologists have placed Monoplacophora, a group of morphologically simple, limpet-like molluscs as sister group to all other conchiferans (shelled molluscs other than Polyplacophora), a grouping that is supported by the latest large-scale phylogenomic study that includes Laevipilina. However, molecular datasets dominated by nuclear ribosomal genes support Monoplacophora + Polyplacophora (Serialia). Here, we evaluate the potential of mitochondrial genome data for resolving placement of Monoplacophora. Results Two complete (Laevipilina antarctica and Vema ewingi) and one partial (Laevipilina hyalina) mitochondrial genomes were sequenced, assembled, and compared. All three genomes show a highly similar architecture including an unusually high number of non-coding regions. Comparison of monoplacophoran gene order shows a gene arrangement pattern not previously reported; there is an inversion of one large gene cluster. Our reanalyses of recently published polyplacophoran mitogenomes show, however, that this feature is also present in some chiton species. Maximum Likelihood and Bayesian Inference analyses of 13 mitochondrial protein-coding genes failed to robustly place Monoplacophora and hypothesis testing could not reject any of the evaluated placements of Monoplacophora. Conclusions Under both serialian or aculiferan-conchiferan scenarios, the observed gene cluster inversion appears to be a convergent evolution of gene arrangements in molluscs. Our phylogenetic results are inconclusive and sensitive to taxon sampling. Aculifera (Polyplacophora + Aplacophora) and Conchifera were never recovered. However, some analyses recovered Serialia (Monoplacophora + Polyplacophora), Diasoma (Bivalvia + Scaphopoda) or Pleistomollusca (Bivalvia + Gastropoda). Although we could not shed light on deep evolutionary traits of Mollusca we found unique patterns of gene arrangements that are common to monoplacophoran and chitonine polyplacophoran species but not to acanthochitonine Polyplacophora. Graphical abstract Complete mitochondrial genome of Laevipilina antarctica
format Article in Journal/Newspaper
author I. Stöger
K. Kocot
A. Poustka
N. Wilson
D. Ivanov
K. Halanych
M. Schrödl
author_facet I. Stöger
K. Kocot
A. Poustka
N. Wilson
D. Ivanov
K. Halanych
M. Schrödl
author_sort I. Stöger
title Monoplacophoran mitochondrial genomes: convergent gene arrangements and little phylogenetic signal
title_short Monoplacophoran mitochondrial genomes: convergent gene arrangements and little phylogenetic signal
title_full Monoplacophoran mitochondrial genomes: convergent gene arrangements and little phylogenetic signal
title_fullStr Monoplacophoran mitochondrial genomes: convergent gene arrangements and little phylogenetic signal
title_full_unstemmed Monoplacophoran mitochondrial genomes: convergent gene arrangements and little phylogenetic signal
title_sort monoplacophoran mitochondrial genomes: convergent gene arrangements and little phylogenetic signal
publisher Figshare
publishDate 2016
url https://dx.doi.org/10.6084/m9.figshare.c.3647534.v1
https://figshare.com/collections/Monoplacophoran_mitochondrial_genomes_convergent_gene_arrangements_and_little_phylogenetic_signal/3647534/1
genre Antarc*
Antarctica
genre_facet Antarc*
Antarctica
op_relation https://dx.doi.org/10.1186/s12862-016-0829-3
https://dx.doi.org/10.6084/m9.figshare.c.3647534
op_rights CC BY 4.0
https://creativecommons.org/licenses/by/4.0
op_rightsnorm CC-BY
op_doi https://doi.org/10.6084/m9.figshare.c.3647534.v1
https://doi.org/10.1186/s12862-016-0829-3
https://doi.org/10.6084/m9.figshare.c.3647534
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