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, 112 (18), 5773-8

Error, Signal, and the Placement of Ctenophora Sister to All Other Animals

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Error, Signal, and the Placement of Ctenophora Sister to All Other Animals

Nathan V Whelan et al. Proc Natl Acad Sci U S A.

Abstract

Elucidating relationships among early animal lineages has been difficult, and recent phylogenomic analyses place Ctenophora sister to all other extant animals, contrary to the traditional view of Porifera as the earliest-branching animal lineage. To date, phylogenetic support for either ctenophores or sponges as sister to other animals has been limited and inconsistent among studies. Lack of agreement among phylogenomic analyses using different data and methods obscures how complex traits, such as epithelia, neurons, and muscles evolved. A consensus view of animal evolution will not be accepted until datasets and methods converge on a single hypothesis of early metazoan relationships and putative sources of systematic error (e.g., long-branch attraction, compositional bias, poor model choice) are assessed. Here, we investigate possible causes of systematic error by expanding taxon sampling with eight novel transcriptomes, strictly enforcing orthology inference criteria, and progressively examining potential causes of systematic error while using both maximum-likelihood with robust data partitioning and Bayesian inference with a site-heterogeneous model. We identified ribosomal protein genes as possessing a conflicting signal compared with other genes, which caused some past studies to infer ctenophores and cnidarians as sister. Importantly, biases resulting from elevated compositional heterogeneity or elevated substitution rates are ruled out. Placement of ctenophores as sister to all other animals, and sponge monophyly, are strongly supported under multiple analyses, herein.

Keywords: Cnidaria; Ctenophora; Metazoa; Porifera; phylogenomics.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Phylogenetic hypotheses from previous molecular studies. (A) Placozoa-sister hypothesis (2). (B) Ctenophora-sister hypothesis (–7). Placozoa was not included in some studies that found support for this topology. (C) Ctenophora + Porifera-sister hypothesis (6). (D) Traditional Porifera-sister hypothesis (–10).
Fig. 2.
Fig. 2.
Hierarchy of datasets with progressive data filtering. Numbers associated with each datasets are references throughout the text. Datasets 5, 11, 15, 21 have Choanoflagellates as an outgroup, and datasets 22, 23, 24, 25 have all outgroups removed. RAxML analyses were used for each dataset, and shaded datasets were also analyzed with PhyloBayes. Data matrix statistics (e.g., number of sites, percentage of missing data, and so forth) for each dataset can be found in Table S2.
Fig. 3.
Fig. 3.
Reconstructed maximum-likelihood topology of metazoan relationships inferred with dataset 10. Maximum likelihood and Bayesian topologies inferred with other datasets (Fig. 2) have identical basal branching patterns (Figs. S1–S5). Nodes are supported with 100% bootstrap support unless otherwise noted. Support, as inferred from each dataset (Fig. 2), for nodes covered by black boxes are in Table 1.

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