Lack of support for Deuterostomia prompts reinterpretation of the first Bilateria

Abstract

<jats:title>Abstract</jats:title><jats:p>The bilaterally symmetric animals (Bilateria) are considered to comprise two monophyletic groups, Protostomia and Deuterostomia. Protostomia contains the Ecdysozoa and the Lophotrochozoa; Deuterostomia contains the Chordata and the Xenambulacraria (Hemichordata, Echinodermata and Xenacoelomorpha). Their names refer to a supposed distinct origin of the mouth (stoma) in the two clades, but these groups have been differentiated by other embryological characters including embryonic cleavage patterns and different ways of forming their mesoderm and coeloms. Deuterostome monophyly is not consistently supported by recent studies. Here we compare support for Protostomia and Deuterostomia using five recently published, phylogenomic datasets. Protostomia is always strongly supported, especially by longer and higher quality genes. Support for Deuterostomia is always equivocal and barely higher than support for paraphyletic alternatives. Conditions that can cause tree reconstruction errors - inadequate models, short internal branch, faster evolving genes, and unequal branch lengths - correlate with statistical support for monophyletic deuterostomes. Simulation experiments show that support for Deuterostomia could be explained by systematic error. A survey of molecular characters supposedly diagnostic of deuterostomes shows many are not valid synapomorphies. The branch between bilaterian and deuterostome common ancestors, if real, is very short. This finding fits with growing evidence suggesting the common ancestor of all Bilateria had many deuterostome characteristics. This finding has important implications for our understanding of early animal evolution and for the interpretation of some enigmatic Cambrian fossils such as vetulicolians and banffiids.</jats:p>

The evolutionary emergence of land plants

“…These biases include differences in nucleotide and amino acid substitution rates between sites within the genome and between evolutionary lineages, which are not addressed in the homogeneous substitution models conventionally employed in molecular phylogenetics. Such biases have impacted some of the highest profile controversies in phylogenetics, including the relationships among ctenophores and sponges with respect to other animals 27 , the fundamental relationships among mammals 28 , and the coherence of some animal supergroups 29 . Cox and colleagues 30,31 have shown that support for bryophyte paraphyly in legacy plastid datasets 22,23 is an artefact of among-lineage compositional heterogeneity -biases in the use of related codons by different sites within the genome.…”

Molecular evidence for a single origin of ultrafiltration-based excretory organs

“…These data support the idea that the conserved set of nephridial developmental TFs has been inherited from the last common ancestor of protostomes and deuterostomes (Figure 4A). Although recently the basal position of Xenacoelomorpha in the bilaterian tree of life has been challenged again 12,13 and monophyly of deuterostomes has been questioned, 51 these ambiguities do not directly influence our reconstruction of the ancestral set of nephridia-related transcription factors. Regardless of the topological controversies, the demonstrated molecular similarities could be traced back to the last common ancestor of protostomes and Ambulacraria (Figure 4A), in which the ancestral excretory organs were already present.…”

Enriching for orthologs increases support for Xenacoelomorpha and Ambulacraria sister relationship

“…the loss such as complex organ systems, a digestive system with mouth and anus, coeloms, and body compartmentalisation (Bourlat et al 2003(Bourlat et al , 2006Philippe, Brinkmann, Copley, et al 2011;Philippe et al 2019;Kapli & Telford 2020). More recently, the placement of Xenacoelomorpha within Bilateria has brought into question whether Deuterostomia should be considered monophyletic at all (Philippe et al 2019;Kapli et al 2021). The paraphyletic Deuterostomia hypothesis places Chordata as sister to Protostomia to the exclusion of Xenambulacraria (Xenacoelomorpha plus Ambulacraria) (Figure 1C), suggesting that the common ancestor of all Bilateria possessed many deuterostome traits such as radial cleavage and the development of the anus from the blastopore, and that these traits were significantly altered or lost at the emergence of Protostomia (Kapli et al 2021).…”

“…More recently, the placement of Xenacoelomorpha within Bilateria has brought into question whether Deuterostomia should be considered monophyletic at all (Philippe et al 2019;Kapli et al 2021). The paraphyletic Deuterostomia hypothesis places Chordata as sister to Protostomia to the exclusion of Xenambulacraria (Xenacoelomorpha plus Ambulacraria) (Figure 1C), suggesting that the common ancestor of all Bilateria possessed many deuterostome traits such as radial cleavage and the development of the anus from the blastopore, and that these traits were significantly altered or lost at the emergence of Protostomia (Kapli et al 2021). Empirical analyses of newly generated genomic and transcriptomic data continue to produce conflicting placements for Xenacoelomorpha, with support garnered for both the Nephrozoa (Figure 1A) (Cannon et al 2016;Rouse et al 2016) and the Xenambulacraria (Figure 1B & C) (Philippe et al 2019) hypotheses.…”