Phylogenetic placement of the enigmatic parasite, Polypodium hydriforme, within the Phylum Cnidaria

Abstract

BackgroundPolypodium hydriforme is a parasite with an unusual life cycle and peculiar morphology, both of which have made its systematic position uncertain. Polypodium has traditionally been considered a cnidarian because it possesses nematocysts, the stinging structures characteristic of this phylum. However, recent molecular phylogenetic studies using 18S rDNA sequence data have challenged this interpretation, and have shown that Polypodium is a close relative to myxozoans and together they share a closer affinity to bilaterians than cnidarians. Due to the variable rates of 18S rDNA sequences, these results have been suggested to be an artifact of long-branch attraction (LBA). A recent study, using multiple protein coding markers, shows that the myxozoan Buddenbrockia, is nested within cnidarians. Polypodium was not included in this study. To further investigate the phylogenetic placement of Polypodium, we have performed phylogenetic analyses of metazoans with 18S and partial 28S rDNA sequences in a large dataset that includes Polypodium and a comprehensive sampling of cnidarian taxa.ResultsAnalyses of a combined dataset of 18S and partial 28S sequences, and partial 28S alone, support the placement of Polypodium within Cnidaria. Removal of the long-branched myxozoans from the 18S dataset also results in Polypodium being nested within Cnidaria. These results suggest that previous reports showing that Polypodium and Myxozoa form a sister group to Bilateria were an artifact of long-branch attraction.ConclusionBy including 28S rDNA sequences and a comprehensive sampling of cnidarian taxa, we demonstrate that previously conflicting hypotheses concerning the phylogenetic placement of Polypodium can be reconciled. Specifically, the data presented provide evidence that Polypodium is indeed a cnidarian and is either the sister taxon to Hydrozoa, or part of the hydrozoan clade, Leptothecata. The former hypothesis is consistent with the traditional view that Polypodium should be placed in its own cnidarian class, Polypodiozoa.

Genomic insights into the evolutionary origin of Myxozoa within Cnidaria

“…We recover P. hydriforme as the sister taxon to Myxozoa and can confirm, with an increased sampling and thus a higher degree of confidence, the placement of this clade as the sister taxon to medusozoan cnidarians. These results are consistent with those of other molecular phylogenetic studies (19,23), although these have been criticized as possible artifacts of long-branch attraction (21). The monophyly of Myxozoa + P. hydriforme is also supported by endoparasitism in fish, a unique cell-within-cell developmental stage, possession of a single similar type of nematocyst (19,23), and similarity in minicollagen sequences (28).…”

“…position of this clade was unstable. It was either placed as the sister clade to Bilateria or nested within Cnidaria, depending on taxon sampling, alignment, optimization method, and the characters considered (13,(19)(20)(21)(22)(23). Recent phylogenomic studies support a position of Myxozoa within Cnidaria, as the sister clade to Medusozoa (24)(25)(26).…”

Phylogenetics of Hydroidolina (Hydrozoa: Cnidaria)

“…An approximately 1.8 kb portion of the gene coding for 18S was amplified with universal eukaryotic primers as described by Medlin et al (1988). Nearly complete, an approximately 3 kb portion of the gene coding for 28S was amplified and sequenced according to Evans et al (2008).…”

A novel minicollagen gene links cnidarians and myxozoans

“…A recent phylogenomic study based on analyses of 50 protein-coding genes [12] provided evidence that myxozoans group within the cnidarians and demonstrated the contaminant nature of Hox genes suggestive of a bilaterian affinity [13]. However, scepticism regarding myxozoan affinities remains owing to limitations of the phylogenomic study, including problems of missing data, bootstrap support of only 70 per cent, an inability to reject alternative placements under certain models, inclusion of only a small number of cnidarians and the absence of P. hydriforme genes in analyses [11,14,15]. In addition, longitudinal muscles in the worm-like myxozoan Buddenbrockia plumatellae occur as independent blocks of muscles typical of mesoderm [16], a body layer putatively lacking in cnidarians [17].…”

“…Myxozoans were long classified as protists because of their extreme morphological degeneracy, but 18S rDNA sequence data and demonstration of multicellularity eventually confirmed a metazoan affinity [9,10]. Subsequent phylogenetic analyses based on 18S rDNA grouped myxozoans variously as a sister taxon to the Bilateria or within the Cnidaria, reflecting the extreme sequence divergence of the Myxozoa and whether the aberrant Polypodium hydriforme (a cnidarian intracellular parasite of oocytes of acipenseriform fish) was included in analyses [11]. A recent phylogenomic study based on analyses of 50 protein-coding genes [12] provided evidence that myxozoans group within the cnidarians and demonstrated the contaminant nature of Hox genes suggestive of a bilaterian affinity [13].…”