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Concatenated analysis sheds light on early metazoan evolution and fuels a modern "urmetazoon" hypothesis.

Schierwater B, Eitel M, Jakob W, Osigus HJ, Hadrys H, Dellaporta SL, Kolokotronis SO, Desalle R - PLoS Biol. (2009)

Bottom Line: Unfortunately, the phylogenetic relationships at the base of Metazoa have been controversial because of conflicting phylogenetic scenarios generated while addressing the question.Here, we analyze the sum of morphological evidence, the secondary structure of mitochondrial ribosomal genes, and molecular sequence data from mitochondrial and nuclear genes that amass over 9,400 phylogenetically informative characters from 24 to 73 taxa.Together with mitochondrial DNA genome structure and sequence analyses and Hox-like gene expression patterns, these data (1) provide evidence that Placozoa are basal relative to all other diploblast phyla and (2) spark a modernized "urmetazoon" hypothesis.

View Article: PubMed Central - PubMed

Affiliation: ITZ, Ecology and Evolution, Tierärztliche Hochschule Hannover, Hannover, Germany. bernd.schierwater@ecolevol.de

ABSTRACT
For more than a century, the origin of metazoan animals has been debated. One aspect of this debate has been centered on what the hypothetical "urmetazoon" bauplan might have been. The morphologically most simply organized metazoan animal, the placozoan Trichoplax adhaerens, resembles an intriguing model for one of several "urmetazoon" hypotheses: the placula hypothesis. Clear support for a basal position of Placozoa would aid in resolving several key issues of metazoan-specific inventions (including, for example, head-foot axis, symmetry, and coelom) and would determine a root for unraveling their evolution. Unfortunately, the phylogenetic relationships at the base of Metazoa have been controversial because of conflicting phylogenetic scenarios generated while addressing the question. Here, we analyze the sum of morphological evidence, the secondary structure of mitochondrial ribosomal genes, and molecular sequence data from mitochondrial and nuclear genes that amass over 9,400 phylogenetically informative characters from 24 to 73 taxa. Together with mitochondrial DNA genome structure and sequence analyses and Hox-like gene expression patterns, these data (1) provide evidence that Placozoa are basal relative to all other diploblast phyla and (2) spark a modernized "urmetazoon" hypothesis.

Show MeSH
Maximum Likelihood Phylogenetic Tree of Metazoan Relationships Using the Concatenated Data MatrixNode support is based on the best ML tree filtered through 1,000 rapid bootstrap replicates. Only support values below 100% are shown. Bayesian inference supported strongly (posterior probability = 1.0) all nodes with the exception of monophyly of Cnidaria. The maximum a posteriori and the Bayesian 50% majority-rule consensus trees disagreed with the best ML tree in supporting a Ctenophora–Anthozoa clade with posterior probability of 0.98. Please note that “Coelenterata” is not a taxonomic unit, but rather it is a traditional grouping for reasons of convenience. The alpha shape parameters of the Gamma distribution were 0.507454 and 0.651659 for the nucleotide and amino acid partitions, respectively. Log-likelihood = −261429.821426.
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pbio-1000020-g002: Maximum Likelihood Phylogenetic Tree of Metazoan Relationships Using the Concatenated Data MatrixNode support is based on the best ML tree filtered through 1,000 rapid bootstrap replicates. Only support values below 100% are shown. Bayesian inference supported strongly (posterior probability = 1.0) all nodes with the exception of monophyly of Cnidaria. The maximum a posteriori and the Bayesian 50% majority-rule consensus trees disagreed with the best ML tree in supporting a Ctenophora–Anthozoa clade with posterior probability of 0.98. Please note that “Coelenterata” is not a taxonomic unit, but rather it is a traditional grouping for reasons of convenience. The alpha shape parameters of the Gamma distribution were 0.507454 and 0.651659 for the nucleotide and amino acid partitions, respectively. Log-likelihood = −261429.821426.

Mentions: Parsimony, likelihood (with morphological characters removed), and mixed Bayesian analysis of the smaller concatenated matrix using a variety of approaches, weighting schemes, and models is generally consistent with the view that Bilateria and diploblasts (Porifera, Ctenophora, Placozoa, and Cnidaria) are sister groups. In addition, Placozoa are robustly observed as the most basal diploblast group (Figure 2 and Figure 3). Figure 3 shows the support for several hypotheses of monophyly obtained from diverse methods of analysis. Porifera, Bilateria, and Fungi all form strong monophyletic groups (Figure 3). The four cnidarian classes (Anthozoa, Hydrozoa, Scyphozoa, and Cubozoa) together with the Ctenophora form a monophyletic group, the “Coelenterata.” Within the Cnidaria, the generally accepted basal position of the anthozoans is also recovered by this analysis [34,35]. Both choanoflagellates and Placozoa are strongly excluded from a Porifera–Coelenterata monophyletic group. The basal position of Placozoa is also strongly supported by comparing the phylogeny in Figure 2 with hypotheses that place it more derived, using the statistical approach of Shimodaira and Hasegawa [36,37]. This battery of tests (Table 1) demonstrates that the basal position of the Placozoa is significantly better than other hypotheses. The 95% confidence tree includes the Maximum Likelihood (ML) and Bayesian trees (both with Placozoa as basal in the diploblasts) with a cumulative expected likelihood weight (ELW) of 0.960763.


Concatenated analysis sheds light on early metazoan evolution and fuels a modern "urmetazoon" hypothesis.

Schierwater B, Eitel M, Jakob W, Osigus HJ, Hadrys H, Dellaporta SL, Kolokotronis SO, Desalle R - PLoS Biol. (2009)

Maximum Likelihood Phylogenetic Tree of Metazoan Relationships Using the Concatenated Data MatrixNode support is based on the best ML tree filtered through 1,000 rapid bootstrap replicates. Only support values below 100% are shown. Bayesian inference supported strongly (posterior probability = 1.0) all nodes with the exception of monophyly of Cnidaria. The maximum a posteriori and the Bayesian 50% majority-rule consensus trees disagreed with the best ML tree in supporting a Ctenophora–Anthozoa clade with posterior probability of 0.98. Please note that “Coelenterata” is not a taxonomic unit, but rather it is a traditional grouping for reasons of convenience. The alpha shape parameters of the Gamma distribution were 0.507454 and 0.651659 for the nucleotide and amino acid partitions, respectively. Log-likelihood = −261429.821426.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2631068&req=5

pbio-1000020-g002: Maximum Likelihood Phylogenetic Tree of Metazoan Relationships Using the Concatenated Data MatrixNode support is based on the best ML tree filtered through 1,000 rapid bootstrap replicates. Only support values below 100% are shown. Bayesian inference supported strongly (posterior probability = 1.0) all nodes with the exception of monophyly of Cnidaria. The maximum a posteriori and the Bayesian 50% majority-rule consensus trees disagreed with the best ML tree in supporting a Ctenophora–Anthozoa clade with posterior probability of 0.98. Please note that “Coelenterata” is not a taxonomic unit, but rather it is a traditional grouping for reasons of convenience. The alpha shape parameters of the Gamma distribution were 0.507454 and 0.651659 for the nucleotide and amino acid partitions, respectively. Log-likelihood = −261429.821426.
Mentions: Parsimony, likelihood (with morphological characters removed), and mixed Bayesian analysis of the smaller concatenated matrix using a variety of approaches, weighting schemes, and models is generally consistent with the view that Bilateria and diploblasts (Porifera, Ctenophora, Placozoa, and Cnidaria) are sister groups. In addition, Placozoa are robustly observed as the most basal diploblast group (Figure 2 and Figure 3). Figure 3 shows the support for several hypotheses of monophyly obtained from diverse methods of analysis. Porifera, Bilateria, and Fungi all form strong monophyletic groups (Figure 3). The four cnidarian classes (Anthozoa, Hydrozoa, Scyphozoa, and Cubozoa) together with the Ctenophora form a monophyletic group, the “Coelenterata.” Within the Cnidaria, the generally accepted basal position of the anthozoans is also recovered by this analysis [34,35]. Both choanoflagellates and Placozoa are strongly excluded from a Porifera–Coelenterata monophyletic group. The basal position of Placozoa is also strongly supported by comparing the phylogeny in Figure 2 with hypotheses that place it more derived, using the statistical approach of Shimodaira and Hasegawa [36,37]. This battery of tests (Table 1) demonstrates that the basal position of the Placozoa is significantly better than other hypotheses. The 95% confidence tree includes the Maximum Likelihood (ML) and Bayesian trees (both with Placozoa as basal in the diploblasts) with a cumulative expected likelihood weight (ELW) of 0.960763.

Bottom Line: Unfortunately, the phylogenetic relationships at the base of Metazoa have been controversial because of conflicting phylogenetic scenarios generated while addressing the question.Here, we analyze the sum of morphological evidence, the secondary structure of mitochondrial ribosomal genes, and molecular sequence data from mitochondrial and nuclear genes that amass over 9,400 phylogenetically informative characters from 24 to 73 taxa.Together with mitochondrial DNA genome structure and sequence analyses and Hox-like gene expression patterns, these data (1) provide evidence that Placozoa are basal relative to all other diploblast phyla and (2) spark a modernized "urmetazoon" hypothesis.

View Article: PubMed Central - PubMed

Affiliation: ITZ, Ecology and Evolution, Tierärztliche Hochschule Hannover, Hannover, Germany. bernd.schierwater@ecolevol.de

ABSTRACT
For more than a century, the origin of metazoan animals has been debated. One aspect of this debate has been centered on what the hypothetical "urmetazoon" bauplan might have been. The morphologically most simply organized metazoan animal, the placozoan Trichoplax adhaerens, resembles an intriguing model for one of several "urmetazoon" hypotheses: the placula hypothesis. Clear support for a basal position of Placozoa would aid in resolving several key issues of metazoan-specific inventions (including, for example, head-foot axis, symmetry, and coelom) and would determine a root for unraveling their evolution. Unfortunately, the phylogenetic relationships at the base of Metazoa have been controversial because of conflicting phylogenetic scenarios generated while addressing the question. Here, we analyze the sum of morphological evidence, the secondary structure of mitochondrial ribosomal genes, and molecular sequence data from mitochondrial and nuclear genes that amass over 9,400 phylogenetically informative characters from 24 to 73 taxa. Together with mitochondrial DNA genome structure and sequence analyses and Hox-like gene expression patterns, these data (1) provide evidence that Placozoa are basal relative to all other diploblast phyla and (2) spark a modernized "urmetazoon" hypothesis.

Show MeSH