Phoronid phylogenetics (Brachiopoda; Phoronata): evidence from morphological cladistics, small and large subunit rDNA sequences, and mitochondrialcox1

Abstract

A matrix of 24 morphodevelopmental characters and an alignment of small subunit (SSU) and large subunit (LSU) rDNA nuclear and cox1 mitochondrial gene sequences (~4500 sites) were compiled from up to 12 phoronids including most named taxa, but probably constituting only a portion of worldwide diversity. Morphological data were analysed by weighted parsimony; sequence data by maximum and Bayesian likelihood, both with Phoronis ovalis as the local outgroup. Morphological and sequence-based phylogenies were similar, but not fully congruent. Phoronid rDNAs were almost free from mutational saturation, but cox1 showed strong saturation unless distant outgroups and P. ovalis were omitted, suggesting that many phoronid divergences are old (Ն100 Myr). rDNA divergence between named phoronid taxa is generally substantial, but Phoronopsis harmeri (from Vladivostock) and Phoronopsis viridis (from California) are genetically close enough to be conspecific. In another alignment, of 24 taxa, phoronid rDNAs were combined with data from brachiopods and distant (molluscan) outgroups. The relative ages of divergence between phoronids and their brachiopod sister-groups, of the split between the P. ovalis and non-ovalis lineages, and of other phoronid splits, were estimated from this alignment with a Bayesian lognormal uncorrelated molecular clock model. Although confidence limits (95% highest probability density) are wide, the results are compatible with an Early Cambrian split between phoronids and brachiopods and with the Upper Devonian latest age suggested for the P. ovalis/non-ovalis split by the putative phoronid ichnofossil, Talpina. Most other ingroup splits appear to be~50-200 Myr old. Inclusion of phoronids with brachiopods in the crown clade pan-Brachiopoda suggests that a distinctive metamorphosis and absence of mineralization are ancestral phoronid apomorphies. Worldwide diversity and possible associations between character-states and life-history attributes deserve comprehensive further study.

Phylogenomics of Lophotrochozoa with Consideration of Systematic Error

“…Although we sampled only four brachiopods, we sampled all major lineages and all of our results are in contrast to studies recovering Phoronida as a subclade of Brachiopoda (Cohen, 2000(Cohen, , 2013 Cohen and Weydmann, 2005;Santagata and Cohen, 2009). …”

“…Although both phyla have a prominent circulatory system in larger animals, the developmental origins and 1995; Dunn et al 2008;Paps et al 2009aPaps et al , 2009bHausdorf et al 2010;Sperling et al 2011). Although we sampled only four brachiopods, we sampled all major lineages and all of our results are in contrast to studies recovering Phoronida as a subclade of Brachiopoda (Cohen, 2000(Cohen, , 2013 Cohen and Weydmann, 2005;Santagata and Cohen, 2009). …”

Phoronida

“…Interestingly, a recent phylogenomic study supports the monophyly of all three lophophore-bearing phyla in which phoronids are closely related to brachiopods and considered an ancestral sister taxon to ectoprocts (Nesnidal et al 2013 ). Species-and genus-level relationships among phoronids based on either morphological or molecular characters are moderately congruent (Santagata and Cohen 2009 ) and support Phoronis ovalis as a divergent lineage, a Phoronopsis clade and a subclade of Phoronis spp. It should be noted that the molecular phylogenetic data discussed here are comprised largely of ribosomal and mitochondrial markers, and a more recent phylogenetic analysis of phoronid species based on these genes plus additional nuclear and mitochondrial genes resolves previously incongruent aspects of the morphology-and molecularbased evolutionary inferences (Santagata, 2014 ).…”

“…Debate still exists as to whether phoronids should be considered as an ancestral sister taxon to all brachiopods (Sperling et al 2011 ; although see Thomson et al 2014 ) or instead as a subtaxon within the brachiopods as a whole (Cohen and Weydmann 2005 ;Santagata and Cohen 2009 ;Cohen 2013 ). Phoronids are clearly closely related to brachiopods and share evolutionary affi nities with spiralian protostomes such as nemerteans, annelids, and mollusks, but their phylogenetic position relative to ectoprocts has been unresolved (Halanych et al 1995 ;Dunn et al 2008 ;Hejnol et al 2009 ;Hausdorf et al 2010 ;Mallatt et al 2012 ).…”

Brachiopoda

“…Although molecular evidence is generally congruent with the paleontological origin of brachiopods, discrepancies do exist, leaving open the question of whether phoronids should be considered as an ancestral sister taxon to all brachiopods (Sperling et al 2011 ; although see Thomson et al 2014 ) or instead as a subtaxon within the brachiopods as a whole (Cohen and Weydmann 2005 ;Santagata and Cohen 2009 ;Cohen 2013 ). Molecular phylogenetic data support the evolutionary affi nities of brachiopods with spiralian protostomes such as nemerteans, annelids, and mollusks (Halanych et al 1995 ;Dunn et al 2008 ;Hejnol et al 2009 ;Hausdorf et al 2010 ;Mallatt et al 2012 ).…”