Platyzoan Paraphyly Based on Phylogenomic Data Supports a Noncoelomate Ancestry of Spiralia

Abstract

Based on molecular data three major clades have been recognized within Bilateria: Deuterostomia, Ecdysozoa, and Spiralia. Within Spiralia, small-sized and simply organized animals such as flatworms, gastrotrichs, and gnathostomulids have recently been grouped together as Platyzoa. However, the representation of putative platyzoans was low in the respective molecular phylogenetic studies, in terms of both, taxon number and sequence data. Furthermore, increased substitution rates in platyzoan taxa raised the possibility that monophyletic Platyzoa represents an artifact due to long-branch attraction. In order to overcome such problems, we employed a phylogenomic approach, thereby substantially increasing 1) the number of sampled species within Platyzoa and 2) species-specific sequence coverage in data sets of up to 82,162 amino acid positions. Using established and new measures (long-branch score), we disentangled phylogenetic signal from misleading effects such as long-branch attraction. In doing so, our phylogenomic analyses did not recover a monophyletic origin of platyzoan taxa that, instead, appeared paraphyletic with respect to the other spiralians. Platyhelminthes and Gastrotricha formed a monophylum, which we name Rouphozoa. To the exclusion of Gnathifera, Rouphozoa and all other spiralians represent a monophyletic group, which we name Platytrochozoa. Platyzoan paraphyly suggests that the last common ancestor of Spiralia was a simple-bodied organism lacking coelomic cavities, segmentation, and complex brain structures, and that more complex animals such as annelids evolved from such a simply organized ancestor. This conclusion contradicts alternative evolutionary scenarios proposing an annelid-like ancestor of Bilateria and Spiralia and several independent events of secondary reduction.

Spiralian model systems

“…The other group includes the Platyzoa (CavalierSmith, 1998;Giribet et al, 2000), which include Gastrotricha, Platyhelminthes, and the groups comprising the "Gnathozoa" or "Gnathifera" (Gnathostomulida, Micrognathozoa and Rotifera (Syndermata)). More recently, however, an analysis by Struck et al, (2014), which included additional species, suggests that the Platyzoa are paraphyletic. Their data suggest that, with the exclusion of the Gnathifera, the Gastrotricha and Platyhelminthes comprise a monophylum, which they term the "Rouphozoa."…”

Systematics, evolution and phylogeny of Annelida – a morphological perspective

“…Heuer et al (2010) regarded mushroom bodies as an ancient structure already present in the annelid stem species and their absence in many annelids as reductions. Since typical mushroom bodies have only been shown to exist in Nereididae and Aphroditiformia and to a lesser degree in a few other errant taxa, as an alternative it has been proposed that mushroom bodies evolved within Errantia or even in one or some of their subtaxa as well as independently in arthropods (Struck, 2012;Struck et al, 2014). This view is held because so far these structures are unknown in any taxon regarded to be basal in the annelid radiation irrespective of which of the conflicting hypotheses is considered ( fig.…”

Clustered brachiopod Hox genes are not expressed collinearly and are associated with lophotrochozoan novelties

“…Thus, it is not surprising that Hox genes show diverse arrangements regarding their genomic organization and expression profiles in the Spiralia (34), a major animal clade that includes highly disparate developmental strategies and body organizations (35)(36)(37)(38)(39). A striking example of this is the bdelloid rotifer Adineta vaga, which belongs to the Gnathifera, the possible sister group to all remaining Spiralia (38,39).…”

“…A striking example of this is the bdelloid rotifer Adineta vaga, which belongs to the Gnathifera, the possible sister group to all remaining Spiralia (38,39). Owing to reduced tetraploidy, the A. vaga Hox complement includes 24 genes, although it lacks posterior Hox genes and a Hox cluster (40).…”