Support for a clade of Placozoa and Cnidaria in genes with minimal compositional bias

Abstract

The phylogenetic placement of the morphologically simple placozoans is crucial to understanding the evolution of complex animal traits. Here, we examine the influence of adding new genomes from placozoans to a large dataset designed to study the deepest splits in the animal phylogeny. Using site-heterogeneous substitution models, we show that it is possible to obtain strong support, in both amino acid and reduced-alphabet matrices, for either a sister-group relationship between Cnidaria and Placozoa, or for Cnidaria and Bilateria as seen in most published work to date, depending on the orthologues selected to construct the matrix. We demonstrate that a majority of genes show evidence of compositional heterogeneity, and that support for the Cnidaria + Bilateria clade can be assigned to this source of systematic error. In interpreting these results, we caution against a peremptory reading of placozoans as secondarily reduced forms of little relevance to broader discussions of early animal evolution.

Keywords: Bilateria; Cnidaria; Placozoa; Trichoplax; compositional heterogeneity; evolutionary biology; phylogeny.

Figure 1.. Consensus phylogram showing deep metazoan interrelationships under Bayesian phylogenetic inference of the 430-orthologue amino acid matrix, using the CAT + GTR + Г4 mixture model.

All nodes received full posterior probability. Numerical annotations of given nodes represent Extended Quadripartition Internode Certainty (EQP-IC) scores, describing among-gene-tree agreement for both the monophyly of the five major metazoan clades and the given relationships between them in this reference tree. A bar chart on the right depicts the proportion of the total orthologue set each terminal taxon is represented by in the concatenated matrix. ‘Placozoa H1’ in this and all other figures refers to the GRELL isolate sequenced in Srivastava et al., 2008, which has there and elsewhere been referred to as Trichoplax adhaerens, despite the absence of type material linking this name to any modern isolate. Line drawings of clade representatives are taken from the BIODIDAC database (http://biodidac.bio.uottawa.ca/).

Figure 1—figure supplement 1.. Maximum likelihood tree under the C60 +LG + FO + R4 profile mixture model, inferred from the 430-orthologue matrix with full taxon sampling.

Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.

Figure 1—figure supplement 2.. Maximum likelihood tree under a profile mixture model inferred from the 430-orthologue matrix, with only Placozoa H1 used to represent this clade.

Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.

Figure 2.. Consensus phylogram under Bayesian phylogenetic inference under the CAT + GTR + Г4 mixture model, on the 430-orthologue concatenated amino acid matrix, recoded into 6 Dayhoff groups.

Nodes annotated with posterior probability; unannotated nodes received full support.

Figure 3.. Posterior consensus trees from CAT + GTR + Г4 mixture model analysis of a 94,444 amino acid supermatrix derived from the 303 single-copy conserved eukaryotic BUSCO orthologs, analysed in A.

amino acid space or (B) the Dayhoff-6 reduced alphabet space. Nodal support values comprise posterior probabilities; nodes with full support not annotated. Taxon colourings as in previous Figures. (C) Plot of z-scores (summed absolute distance between taxon-specific and global empirical frequencies) from representative posterior predictive tests of amino acid compositional bias, from both the BUSCO 303-orthologue matrix (red) and the initial 430-orthologue matrix (blue). Placozoan taxon abbreviations are shown in blue font.

Figure 4.. Schematic depiction of deep metazoan interrelationships in posterior consensus trees from CAT + GTR + Г4 mixture model analyses of matrices made from subsets of genes passing or failing a sensitive null-simulation test of compositional heterogeneity.

Panels correspond to (A) the amino acid matrix made within the failing set; (B) the amino acid matrix derived from the passing set; (C) the Dayhoff-6 recoded matrix from the failing set; (D) the Dayhoff-6 recoded matrix from the passing set. Only nodes with posterior probability less than 1.00 are annotated numerically.

Figure 4—figure supplement 1.. Maximum likelihood tree under a profile mixture model inferred from the 349-orthologue matrix composed from the subset of genes binned as failing the null-simulation compositional bias test.

Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.

Figure 4—figure supplement 2.. Maximum likelihood tree under a profile mixture model inferred from the 348-orthologue matrix composed from the subset of genes binned as passing the null-simulation compositional bias test.

Nodes annotated with ultrafast bootstrap supports with NNI correction; unannotated nodes received full support.

Author response image 1.