Error, signal, and the placement of Ctenophora sister to all other animals

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., longbranch 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.phylogenomics | Metazoa | Ctenophora | Porifera | Cnidaria R esolving relationships among extant lineages at the base of the metazoan tree is integral to understanding evolution of complex animal traits, including nervous systems and gastrulation. Historically, sponges and placozoans, both of which have relatively simple body plans and lack neurons, have been considered to diverge from other animals earlier than ctenophores, cnidarians, and bilaterians (1). Phylogenomic studies have resulted in controversial hypotheses placing either Placozoa (Fig. 1A) (2), ctenophores (ctenophore-sister hypothesis) (Fig. 1B) (3-7), or a clade of ctenophores and sponges (Fig. 1C) (6) as sister to all remaining animals. Others (7-10) have claimed nontraditional findings resulted from systematic error and argued for traditional placement of sponges as sister to all remaining animals (Eumetazoa, or Porifera-sister hypothesis) (Fig. 1D) and a sister relationship between ctenophores and cnidarians (Coelenterata) (Fig. 1D). Limited statistical support for various hypotheses and conflict among, and even within studies, has undermined confidence in our understanding of early animal evolution. Basal metazoan relationships must be resolved with greater consistency before a consensus viewpoint is widely accepted.Long-branch attraction (LBA) (11), which occurs when two divergent lineages are artificially inferred as related because of substitutional saturation (11), is p...

Genomic data do not support comb jellies as the sister group to all other animals

“…We performed outgroup subsampling analogous to Ryan et al (4) on both of these datasets and analyzed the resulting six datasets under the siteheterogeneous CAT model (Methods). Consistent with our results from the Ryan et al (4) datasets, analysis of the Whelan et al (6) datasets gave decreased support for Ctenophora-sister because distantly related outgroups were excluded (Fig. 2 and Figs.…”

“…Although Ryan-Opistho still supported Ctenophora-sister (Fig. S1A), Ryan-Holo and Ryan-Choano (6). Higher scores indicate a better empirical fit.…”

“…That is, all of the outgroup-subsampled datasets were analyzed exclusively using site-homogeneous substitution models, whereas the analyses using the better-fitting site-heterogeneous model were exclusively performed using the full set of outgroups, which included distantly related Fungi. We chose to base our analyses on their two most stringent datasets (Whelan-6 and Whelan-16; details are provided in Methods), because Whelan et al (6) argue that these datasets are the most robust to systematic errors. Furthermore, these datasets were the only ones they analyzed with a site-heterogeneous model of sequence evolution (CAT-GTR).…”

“…Although results from the first study supporting Ctenophorasister (2) were questioned soon thereafter and suggested to be an artifact stemming from the inclusion of too few nonbilaterian species (12) and the use of too rapidly evolving genes (13), this hypothesis has recently been revived in several studies, including analyses of the first two complete ctenophore nuclear genomes, as well as transcriptomic datasets from numerous other ctenophore species (4)(5)(6). Here, we present analyses of key datasets from Ryan et al (4), Moroz et al (5), and Whelan et al (6), and identify several problems in these studies, specifically the combined use of relatively simplistic models of molecular…”

“…Here, we present analyses of key datasets from Ryan et al (4), Moroz et al (5), and Whelan et al (6), and identify several problems in these studies, specifically the combined use of relatively simplistic models of molecular…”