Molecular evidence that phoronids are a subtaxon of brachiopods (Brachiopoda: Phoronata) and that genetic divergence of metazoan phyla began long before the early Cambrian

Abstract

Concatenated SSU (18S) and partial LSU (28S) sequences ($2 kb) from 12 ingroup taxa, comprising 2 phoronids, 2 members of each of the craniid, discinid, and lingulid inarticulate brachiopod lineages, and 4 rhynchonellate, articulate brachiopods (2 rhynchonellides, 1 terebratulide and 1 terebratellide) were aligned with homologous sequences from 6 protostome, deuterostome and sponge outgroups (3964 sites). Regions of potentially ambiguous alignment were removed, and the resulting data (3275 sites, of which 377 were parsimony-informative and 635 variable) were analysed by parsimony, and by maximum and Bayesian likelihood using objectively selected models. There was no base composition heterogeneity. Relative rate tests led to the exclusion (from most analyses) of the more distant outgroups, with retention of the closer pectinid and polyplacophoran (chiton). Parsimony and likelihood bootstrap and Bayesian clade support values were generally high, but only likelihood analyses recovered all brachiopod indicator clades designated a priori. All analyses confirmed the monophyly of (brachiopods+phoronids) and identified phoronids as the sister-group of the three inarticulate brachiopod lineages. Consequently, a revised Linnean classification is proposed in which the subphylum Linguliformea comprises three classes: Lingulata, 'Phoronata' (the phoronids), and 'Craniata' (the current subphylum Craniiformea). Divergence times of all nodes were estimated by regression from node depths in non-parametrically rate-smoothed and other chronograms, calibrated against palaeontological data, with probable errors not less than 50 My. Only three predicted brachiopod divergence times disagree with palaeontological ages by more than the probable error, and a reasonable explanation exists for at least two. Pruning long-branched ingroups made scant difference to predicted divergence time estimates. The palaeontological age calibration and the existence of Lower Cambrian fossils of both main brachiopod clades together indicate that initial genetic divergence between brachiopod and molluscan (chiton) lineages occurred well before the Lower Cambrian, suggesting that much divergence between metazoan phyla took place in the Proterozoic.

The Evolution of Brachiopoda

“…The crown clade of articulated brachiopods has been recently named Neoarticulata (Carlson & Cohen 2016) for the first time, with Pan-Neoarticulata as its associated total clade (Carlson & Cohen 2016) in accordance with phylogenetic nomenclature. Results of molecular analyses support not only the monophyly of the crown clades of Brachiopoda, Inarticulata, and Neoarticulata (Figure 4) but also the monophyly of crown clade Terebratulida, Thecideida, and Rhynchonellida, and within Terebratulida, the monophyly of crown clade Terebratellidina and Terebratulidina (Cohen & Gawthrop 1997;Cohen 2000Cohen , 2007Cohen , 2013Cohen & Weydmann 2005). Total clade monophyly has not been established for most of these groups, however.…”

A Developmental Basis for the Cambrian Radiation

“…This gave a phylum with three closely related subphyla, Linguliformea, Craniiformea, and Phoroniformea, that made up one major clade and the Rhynchonelliformea that made up the other major clade. Subsequent work by Cohen and Weydmann (2005) using both the small subunit and partial large subunits of rDNA sequences showed that the Phoroniformea were the basal members of its clade and that the Linguliformea and Craniiformea were the derived members of that clade (Fig. 1B).…”

“…For extant genera, the time when the order they belong to first appeared and any earlier orders that gave rise to the order they reside in are indicated (adapted from Williams et al, 1996). B) Molecular phylogeny for extant brachiopod subphyla based on the small subunit of rDNA and partial large subunits of rDNA (adapted from Cohen and Weydmann, 2005). the outgroup for the cladistic classification, nested with the Linguliformea and Craniiformea within the phylum Brachiopoda (see Halanych, 2004 for a discussion of earlier work on the phylogenetic affinities of the Phoronida).…”

Evolutionary and Structural Diversification of the Larval Nervous System Among Marine Bryozoans

“…The more divergent morphologies present within the Lophotrochozoa confound traditional evolutionary interpretations of many larval and adult characters, especially with regard to the "lophophorates." More recent studies on the development and larval anatomy of phoronids and brachiopods have expanded our understanding of their evolutionary affinities (Santagata and Zimmer, 2002;Santagata, 2004b;Cohen and Weydmann, 2005). However, often left anatomically and phylogenetically orphaned by these reports, are the bryozoans.…”