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The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes.

Bourlat SJ, Rota-Stabelli O, Lanfear R, Telford MJ - BMC Evol. Biol. (2009)

Bottom Line: Xenoturbella bocki is a morphologically simple benthic marine worm recently found to belong among the deuterostomes.Phylogenetic analyses of the mitochondrial sequence indicate a weakly supported placement as a basal deuterostome, a result that may be the effect of compositional bias.Finally, while phylogenetic analyses of the mitochondrial sequences support a basal deuterostome placement, support for this decreases with the use of more sophisticated models of sequence evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Invertebrate Zoology, Swedish Museum of Natural History, Stockholm, Sweden. sarah.bourlat@nrm.se

ABSTRACT

Background: Mitochondrial genome comparisons contribute in multiple ways when inferring animal relationships. As well as primary sequence data, rare genomic changes such as gene order, shared gene boundaries and genetic code changes, which are unlikely to have arisen through convergent evolution, are useful tools in resolving deep phylogenies. Xenoturbella bocki is a morphologically simple benthic marine worm recently found to belong among the deuterostomes. Here we present analyses comparing the Xenoturbella bocki mitochondrial gene order, genetic code and control region to those of other metazoan groups.

Results: The complete mitochondrial genome sequence of Xenoturbella bocki was determined. The gene order is most similar to that of the chordates and the hemichordates, indicating that this conserved mitochondrial gene order might be ancestral to the deuterostome clade. Using data from all phyla of deuterostomes, we infer the ancestral mitochondrial gene order for this clade. Using inversion and breakpoint analyses of metazoan mitochondrial genomes, we test conflicting hypotheses for the phylogenetic placement of Xenoturbella and find a closer affinity to the hemichordates than to other metazoan groups. Comparative analyses of the control region reveal similarities in the transcription initiation and termination sites and origin of replication of Xenoturbella with those of the vertebrates. Phylogenetic analyses of the mitochondrial sequence indicate a weakly supported placement as a basal deuterostome, a result that may be the effect of compositional bias.

Conclusion: The mitochondrial genome of Xenoturbella bocki has a very conserved gene arrangement in the deuterostome group, strikingly similar to that of the hemichordates and the chordates, and thus to the ancestral deuterostome gene order. Similarity to the hemichordates in particular is suggested by inversion and breakpoint analysis. Finally, while phylogenetic analyses of the mitochondrial sequences support a basal deuterostome placement, support for this decreases with the use of more sophisticated models of sequence evolution.

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Consensus tree from bayesian analyses using different amino acid models. Topology and branch lengths correspond to the consensus tree from a bayesian analysis using the MtHydro model. Values at nodes are the posterior probabilities using the following models from left to right respectively: amino acid functional recoding, MtZoa, MtHydro and the CAT model (in brackets). All models place Xenoturbella as a basal deuterostome. Functional recoding, MtZoa and MtHydro support paraphyletic deuterostomes, due to LBA between the urochordates and the non-bilaterians. The CAT model supports monophyletic deuterostomes, although it groups the urochordates with the echinoderms. Note that the lower the support for paraphyletic deuterostomes, the lower the support for Xenoturbella as basal deuterostome.
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Figure 3: Consensus tree from bayesian analyses using different amino acid models. Topology and branch lengths correspond to the consensus tree from a bayesian analysis using the MtHydro model. Values at nodes are the posterior probabilities using the following models from left to right respectively: amino acid functional recoding, MtZoa, MtHydro and the CAT model (in brackets). All models place Xenoturbella as a basal deuterostome. Functional recoding, MtZoa and MtHydro support paraphyletic deuterostomes, due to LBA between the urochordates and the non-bilaterians. The CAT model supports monophyletic deuterostomes, although it groups the urochordates with the echinoderms. Note that the lower the support for paraphyletic deuterostomes, the lower the support for Xenoturbella as basal deuterostome.

Mentions: Our results show that trees obtained using MrBayes consistently support a basal deuterostome position for Xenoturbella (see figure 3) in accordance with Perseke and colleagues [16]. This hypothesis is strongly supported by using the 4 amino acid functional recoding (99 pp), while, interestingly, using MtZoa (90 pp) and MtHydro (75 pp) the support decreases. In all the tree analyses the urochordates branch with the long branched outgroups, but support for this decreases from using the 4 functional categories (98 pp) to MtZoa (90 pp) and MtHydro (73 pp). We suggest that urochordates may be used here as an internal diagnostic of how the models fit the dataset. We suggest that as the model tends to escape a "wrong" urochordate position (with the outgroups, making chordates polyphyletic), the better the model fits the dataset and reduces the amount of false phylogenetic signal. Interestingly the decrease in support for urochordates+outgroup in the three models (98, 90, 73 respectively for functional recoding, MtZoa and MtHydro) is proportional to the decrease in support for a basal deuterostome position for Xenoturbella (99, 90, 75).


The mitochondrial genome structure of Xenoturbella bocki (phylum Xenoturbellida) is ancestral within the deuterostomes.

Bourlat SJ, Rota-Stabelli O, Lanfear R, Telford MJ - BMC Evol. Biol. (2009)

Consensus tree from bayesian analyses using different amino acid models. Topology and branch lengths correspond to the consensus tree from a bayesian analysis using the MtHydro model. Values at nodes are the posterior probabilities using the following models from left to right respectively: amino acid functional recoding, MtZoa, MtHydro and the CAT model (in brackets). All models place Xenoturbella as a basal deuterostome. Functional recoding, MtZoa and MtHydro support paraphyletic deuterostomes, due to LBA between the urochordates and the non-bilaterians. The CAT model supports monophyletic deuterostomes, although it groups the urochordates with the echinoderms. Note that the lower the support for paraphyletic deuterostomes, the lower the support for Xenoturbella as basal deuterostome.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2697986&req=5

Figure 3: Consensus tree from bayesian analyses using different amino acid models. Topology and branch lengths correspond to the consensus tree from a bayesian analysis using the MtHydro model. Values at nodes are the posterior probabilities using the following models from left to right respectively: amino acid functional recoding, MtZoa, MtHydro and the CAT model (in brackets). All models place Xenoturbella as a basal deuterostome. Functional recoding, MtZoa and MtHydro support paraphyletic deuterostomes, due to LBA between the urochordates and the non-bilaterians. The CAT model supports monophyletic deuterostomes, although it groups the urochordates with the echinoderms. Note that the lower the support for paraphyletic deuterostomes, the lower the support for Xenoturbella as basal deuterostome.
Mentions: Our results show that trees obtained using MrBayes consistently support a basal deuterostome position for Xenoturbella (see figure 3) in accordance with Perseke and colleagues [16]. This hypothesis is strongly supported by using the 4 amino acid functional recoding (99 pp), while, interestingly, using MtZoa (90 pp) and MtHydro (75 pp) the support decreases. In all the tree analyses the urochordates branch with the long branched outgroups, but support for this decreases from using the 4 functional categories (98 pp) to MtZoa (90 pp) and MtHydro (73 pp). We suggest that urochordates may be used here as an internal diagnostic of how the models fit the dataset. We suggest that as the model tends to escape a "wrong" urochordate position (with the outgroups, making chordates polyphyletic), the better the model fits the dataset and reduces the amount of false phylogenetic signal. Interestingly the decrease in support for urochordates+outgroup in the three models (98, 90, 73 respectively for functional recoding, MtZoa and MtHydro) is proportional to the decrease in support for a basal deuterostome position for Xenoturbella (99, 90, 75).

Bottom Line: Xenoturbella bocki is a morphologically simple benthic marine worm recently found to belong among the deuterostomes.Phylogenetic analyses of the mitochondrial sequence indicate a weakly supported placement as a basal deuterostome, a result that may be the effect of compositional bias.Finally, while phylogenetic analyses of the mitochondrial sequences support a basal deuterostome placement, support for this decreases with the use of more sophisticated models of sequence evolution.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Invertebrate Zoology, Swedish Museum of Natural History, Stockholm, Sweden. sarah.bourlat@nrm.se

ABSTRACT

Background: Mitochondrial genome comparisons contribute in multiple ways when inferring animal relationships. As well as primary sequence data, rare genomic changes such as gene order, shared gene boundaries and genetic code changes, which are unlikely to have arisen through convergent evolution, are useful tools in resolving deep phylogenies. Xenoturbella bocki is a morphologically simple benthic marine worm recently found to belong among the deuterostomes. Here we present analyses comparing the Xenoturbella bocki mitochondrial gene order, genetic code and control region to those of other metazoan groups.

Results: The complete mitochondrial genome sequence of Xenoturbella bocki was determined. The gene order is most similar to that of the chordates and the hemichordates, indicating that this conserved mitochondrial gene order might be ancestral to the deuterostome clade. Using data from all phyla of deuterostomes, we infer the ancestral mitochondrial gene order for this clade. Using inversion and breakpoint analyses of metazoan mitochondrial genomes, we test conflicting hypotheses for the phylogenetic placement of Xenoturbella and find a closer affinity to the hemichordates than to other metazoan groups. Comparative analyses of the control region reveal similarities in the transcription initiation and termination sites and origin of replication of Xenoturbella with those of the vertebrates. Phylogenetic analyses of the mitochondrial sequence indicate a weakly supported placement as a basal deuterostome, a result that may be the effect of compositional bias.

Conclusion: The mitochondrial genome of Xenoturbella bocki has a very conserved gene arrangement in the deuterostome group, strikingly similar to that of the hemichordates and the chordates, and thus to the ancestral deuterostome gene order. Similarity to the hemichordates in particular is suggested by inversion and breakpoint analysis. Finally, while phylogenetic analyses of the mitochondrial sequences support a basal deuterostome placement, support for this decreases with the use of more sophisticated models of sequence evolution.

Show MeSH
Related in: MedlinePlus