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EST based phylogenomics of Syndermata questions monophyly of Eurotatoria.

Witek A, Herlyn H, Meyer A, Boell L, Bucher G, Hankeln T - BMC Evol. Biol. (2008)

Bottom Line: Here we present our results from a phylogenomic approach studying i) the phylogenetic position of Syndermata within Spiralia, ii) the monophyletic origin of monogononts and bdelloids and iii) the phylogenetic relations of the latter two taxa to acanthocephalans.Our findings suggest that the phylogenetic position of Syndermata within Spiralia is close to Platyhelminthes, that Eurotatoria are not monophyletic and that bdelloids are more closely related to acanthocephalans than monogononts.Mapping morphological character evolution onto molecular phylogeny suggests the (partial or complete) reduction of the corona and the emergence of a retractable anterior end (rostrum, proboscis) before the separation of Acanthocephala.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular Genetics, Johannes Gutenberg-University Mainz, J. J.-Becherweg 32, D-55099 Mainz, Germany. witeka@uni-mainz.de

ABSTRACT

Background: The metazoan taxon Syndermata comprising Rotifera (in the classical sense of Monogononta+Bdelloidea+Seisonidea) and Acanthocephala has raised several hypotheses connected to the phylogeny of these animal groups and the included subtaxa. While the monophyletic origin of Syndermata and Acanthocephala is well established based on morphological and molecular data, the phylogenetic position of Syndermata within Spiralia, the monophyletic origin of Monogononta, Bdelloidea, and Seisonidea and the acanthocephalan sister group are still a matter of debate. The comparison of the alternative hypotheses suggests that testing the phylogenetic validity of Eurotatoria (Monogononta+Bdelloidea) is the key to unravel the phylogenetic relations within Syndermata. The syndermatan phylogeny in turn is a prerequisite for reconstructing the evolution of the acanthocephalan endoparasitism.

Results: Here we present our results from a phylogenomic approach studying i) the phylogenetic position of Syndermata within Spiralia, ii) the monophyletic origin of monogononts and bdelloids and iii) the phylogenetic relations of the latter two taxa to acanthocephalans. For this analysis we have generated EST libraries of Pomphorhynchus laevis, Echinorhynchus truttae (Acanthocephala) and Brachionus plicatilis (Monogononta). By extending these data with database entries of B. plicatilis, Philodina roseola (Bdelloidea) and 25 additional metazoan species, we conducted phylogenetic reconstructions based on 79 ribosomal proteins using maximum likelihood and bayesian approaches. Our findings suggest that the phylogenetic position of Syndermata within Spiralia is close to Platyhelminthes, that Eurotatoria are not monophyletic and that bdelloids are more closely related to acanthocephalans than monogononts.

Conclusion: Mapping morphological character evolution onto molecular phylogeny suggests the (partial or complete) reduction of the corona and the emergence of a retractable anterior end (rostrum, proboscis) before the separation of Acanthocephala. In particular, the evolution of a rostrum might have been a key event leading to the later evolution of the acanthocephalan endoparasitism, given the enormous relevance of the proboscis for anchoring of the adults to the definitive hosts' intestinal wall.

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Phylogenetic tree reconstruction using bayesian inference (Phylobayes). Numbers at internal nodes represent posterior probabilities. Syndermata are shown as a basal spiralian taxon. Moreover, Eurotatoria appear paraphyletic, with Bdelloidea being more closely related to Acanthocephala than to Monogononta.
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Figure 3: Phylogenetic tree reconstruction using bayesian inference (Phylobayes). Numbers at internal nodes represent posterior probabilities. Syndermata are shown as a basal spiralian taxon. Moreover, Eurotatoria appear paraphyletic, with Bdelloidea being more closely related to Acanthocephala than to Monogononta.

Mentions: Maximum likelihood and bayesian phylogenetic inference consistently support a monophyletic origin of Spiralia, although with partly moderate support values (PhyML < 50; Treefinder: 91; PhyloBayes: 0.93) (Fig. 3, 4, 5). Interestingly, only the PhyloBayes tree depicts the widely accepted monophylum Ecdysozoa (e.g., [16]) so that bayesian inference might provide more reliable results than the maximum likelihood approaches employed, given the present data (Fig. 3). Irrespective of this detail, all three tree reconstruction methods yield maximum support for a monophyletic origin of B. plicatilis, P. roseola, E. truttae and P. laevis and, thus, for the monophyletic origin of the four syndermatan species covered by the present dataset (PhyML: 100; Treefinder: 100, PhyloBayes: 1.00). Within the spiralian clade, Syndermata either group with Platyhelminthes (PhyML: 59; Treefinder: 92) (Fig. 4 and 5) or with a clade comprising Platyhelminthes, Bryozoa, Mollusca and Annelida (PhyloBayes: 0.93) (Fig. 3). Remarkably, none of the tree reconstruction methods supports a sister group relationship of Monogononta and Bdelloidea. Instead, Bdelloidea consistently appear more closely related to Acanthocephala than to Monogononta (PhyML: 78; Treefinder: 76; PhyloBayes: 0.83). The paraphyly of Eurotatoria is further corroborated by results from hypothesis testing. Thereafter, a grouping of Bdelloidea+Acanthocephala is much more likely than the alternatives Monogononta+Bdelloidea and Monogononta+Acanthocephala (Tab. 3). Final evidence for the robustness of the present analysis comes from testing for the effect of missing data in the full-length dataset on the results of tree reconstruction [41]. Thus, the internal syndermatan phylogeny did not change when tree reconstruction was carried out on the basis of a shorter dataset (24 ribosomal proteins, 3,535 amino acid positions) in which all ribosomal protein sequences had orthologs in acanthocephalans, bdelloids and monogononts. Support for a grouping of Bdelloidea and Acanthocephala was even higher when underlying this shorter dataset (PhyML: 83; Treefinder: 85; PhyloBayes: 0.92). Taken together our data suggest i) Syndermata being Spiralia with a close phylogenetic relation to Platyhelminthes and ii) the paraphyly of Eurotatoria, with iii) Bdelloidea being more closely related to Acanthocephala than to Monogononta.


EST based phylogenomics of Syndermata questions monophyly of Eurotatoria.

Witek A, Herlyn H, Meyer A, Boell L, Bucher G, Hankeln T - BMC Evol. Biol. (2008)

Phylogenetic tree reconstruction using bayesian inference (Phylobayes). Numbers at internal nodes represent posterior probabilities. Syndermata are shown as a basal spiralian taxon. Moreover, Eurotatoria appear paraphyletic, with Bdelloidea being more closely related to Acanthocephala than to Monogononta.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2654452&req=5

Figure 3: Phylogenetic tree reconstruction using bayesian inference (Phylobayes). Numbers at internal nodes represent posterior probabilities. Syndermata are shown as a basal spiralian taxon. Moreover, Eurotatoria appear paraphyletic, with Bdelloidea being more closely related to Acanthocephala than to Monogononta.
Mentions: Maximum likelihood and bayesian phylogenetic inference consistently support a monophyletic origin of Spiralia, although with partly moderate support values (PhyML < 50; Treefinder: 91; PhyloBayes: 0.93) (Fig. 3, 4, 5). Interestingly, only the PhyloBayes tree depicts the widely accepted monophylum Ecdysozoa (e.g., [16]) so that bayesian inference might provide more reliable results than the maximum likelihood approaches employed, given the present data (Fig. 3). Irrespective of this detail, all three tree reconstruction methods yield maximum support for a monophyletic origin of B. plicatilis, P. roseola, E. truttae and P. laevis and, thus, for the monophyletic origin of the four syndermatan species covered by the present dataset (PhyML: 100; Treefinder: 100, PhyloBayes: 1.00). Within the spiralian clade, Syndermata either group with Platyhelminthes (PhyML: 59; Treefinder: 92) (Fig. 4 and 5) or with a clade comprising Platyhelminthes, Bryozoa, Mollusca and Annelida (PhyloBayes: 0.93) (Fig. 3). Remarkably, none of the tree reconstruction methods supports a sister group relationship of Monogononta and Bdelloidea. Instead, Bdelloidea consistently appear more closely related to Acanthocephala than to Monogononta (PhyML: 78; Treefinder: 76; PhyloBayes: 0.83). The paraphyly of Eurotatoria is further corroborated by results from hypothesis testing. Thereafter, a grouping of Bdelloidea+Acanthocephala is much more likely than the alternatives Monogononta+Bdelloidea and Monogononta+Acanthocephala (Tab. 3). Final evidence for the robustness of the present analysis comes from testing for the effect of missing data in the full-length dataset on the results of tree reconstruction [41]. Thus, the internal syndermatan phylogeny did not change when tree reconstruction was carried out on the basis of a shorter dataset (24 ribosomal proteins, 3,535 amino acid positions) in which all ribosomal protein sequences had orthologs in acanthocephalans, bdelloids and monogononts. Support for a grouping of Bdelloidea and Acanthocephala was even higher when underlying this shorter dataset (PhyML: 83; Treefinder: 85; PhyloBayes: 0.92). Taken together our data suggest i) Syndermata being Spiralia with a close phylogenetic relation to Platyhelminthes and ii) the paraphyly of Eurotatoria, with iii) Bdelloidea being more closely related to Acanthocephala than to Monogononta.

Bottom Line: Here we present our results from a phylogenomic approach studying i) the phylogenetic position of Syndermata within Spiralia, ii) the monophyletic origin of monogononts and bdelloids and iii) the phylogenetic relations of the latter two taxa to acanthocephalans.Our findings suggest that the phylogenetic position of Syndermata within Spiralia is close to Platyhelminthes, that Eurotatoria are not monophyletic and that bdelloids are more closely related to acanthocephalans than monogononts.Mapping morphological character evolution onto molecular phylogeny suggests the (partial or complete) reduction of the corona and the emergence of a retractable anterior end (rostrum, proboscis) before the separation of Acanthocephala.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Molecular Genetics, Johannes Gutenberg-University Mainz, J. J.-Becherweg 32, D-55099 Mainz, Germany. witeka@uni-mainz.de

ABSTRACT

Background: The metazoan taxon Syndermata comprising Rotifera (in the classical sense of Monogononta+Bdelloidea+Seisonidea) and Acanthocephala has raised several hypotheses connected to the phylogeny of these animal groups and the included subtaxa. While the monophyletic origin of Syndermata and Acanthocephala is well established based on morphological and molecular data, the phylogenetic position of Syndermata within Spiralia, the monophyletic origin of Monogononta, Bdelloidea, and Seisonidea and the acanthocephalan sister group are still a matter of debate. The comparison of the alternative hypotheses suggests that testing the phylogenetic validity of Eurotatoria (Monogononta+Bdelloidea) is the key to unravel the phylogenetic relations within Syndermata. The syndermatan phylogeny in turn is a prerequisite for reconstructing the evolution of the acanthocephalan endoparasitism.

Results: Here we present our results from a phylogenomic approach studying i) the phylogenetic position of Syndermata within Spiralia, ii) the monophyletic origin of monogononts and bdelloids and iii) the phylogenetic relations of the latter two taxa to acanthocephalans. For this analysis we have generated EST libraries of Pomphorhynchus laevis, Echinorhynchus truttae (Acanthocephala) and Brachionus plicatilis (Monogononta). By extending these data with database entries of B. plicatilis, Philodina roseola (Bdelloidea) and 25 additional metazoan species, we conducted phylogenetic reconstructions based on 79 ribosomal proteins using maximum likelihood and bayesian approaches. Our findings suggest that the phylogenetic position of Syndermata within Spiralia is close to Platyhelminthes, that Eurotatoria are not monophyletic and that bdelloids are more closely related to acanthocephalans than monogononts.

Conclusion: Mapping morphological character evolution onto molecular phylogeny suggests the (partial or complete) reduction of the corona and the emergence of a retractable anterior end (rostrum, proboscis) before the separation of Acanthocephala. In particular, the evolution of a rostrum might have been a key event leading to the later evolution of the acanthocephalan endoparasitism, given the enormous relevance of the proboscis for anchoring of the adults to the definitive hosts' intestinal wall.

Show MeSH
Related in: MedlinePlus