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Background: Seisonidea (also Seisonacea or Seisonidae) is a group of small animals living on marine crustaceans (Nebalia spec.) with only four species described so far. Its monophyletic origin with mostly free-living wheel animals (Monogononta, Bdelloidea) and endoparasitic thorny-headed worms (Acanthocephala) is widely accepted. However, the phylogenetic relationships inside the Rotifera-Acanthocephala clade (Rotifera sensu lato or Syndermata) are subject to ongoing debate, with consequences for our understanding of how genomes and lifestyles might have evolved. To gain new insights, we analyzed first drafts of the genome and transcriptome of the key taxon Seisonidea., Results: Analyses of gDNA-Seq and mRNA-Seq data uncovered two genetically distinct lineages in Seison nebaliae Grube, 1861 off the French Channel coast. Their mitochondrial haplotypes shared only 82% sequence identity despite identical gene order. In the nuclear genome, distinct linages were reflected in different gene compactness, GC content and codon usage. The haploid nuclear genome spans ca. 46 Mb, of which 96% were reconstructed. According to ~ 23,000 SuperTranscripts, gene number in S. nebaliae should be within the range published for other members of Rotifera-Acanthocephala. Consistent with this, numbers of metazoan core orthologues and ANTP-type transcriptional regulatory genes in the S. nebaliae genome assembly were between the corresponding numbers in the other assemblies analyzed. We additionally provide evidence that a basal branching of Seisonidea within Rotifera-Acanthocephala could reflect attraction to the outgroup. Accordingly, rooting via a reconstructed ancestral sequence led to monophyletic Pararotatoria (Seisonidea+Acanthocephala) within Hemirotifera (Bdelloidea+Pararotatoria)., Conclusion: Matching genome/transcriptome metrics with the above phylogenetic hypothesis suggests that a haploid nuclear genome of about 50 Mb represents the plesiomorphic state for Rotifera-Acanthocephala. Smaller genome size in S. nebaliae probably results from subsequent reduction. In contrast, genome size should have increased independently in monogononts as well as bdelloid and acanthocephalan stem lines. The present data additionally indicate a decrease in gene repertoire from free-living to epizoic and endoparasitic lifestyles. Potentially, this reflects corresponding steps from the root of Rotifera-Acanthocephala via the last common ancestors of Hemirotifera and Pararotatoria to the one of Acanthocephala. Lastly, rooting via a reconstructed ancestral sequence may prove useful in phylogenetic analyses of other deep splits., (© 2021. The Author(s).)

A monophyletic origin of endoparasitic thorny-headed worms (Acanthocephala) and wheel-animals (Rotifera) is widely accepted. However, the phylogeny inside the clade, be it called Syndermata or Rotifera, has lacked validation by mitochondrial (mt) data. Herein, we present the first mt genome of the key taxon Seison and report conflicting results of phylogenetic analyses: while mt sequence-based topologies showed monophyletic Lemniscea (Bdelloidea+Acanthocephala), gene order analyses supported monophyly of Pararotatoria (Seisonidea+Acanthocephala) and Hemirotifera (Bdelloidea+Pararotatoria). Sequence-based analyses obviously suffered from substitution saturation, compositional bias, and branch length heterogeneity; however, we observed no compromising effects in gene order analyses. Moreover, gene order-based topologies were robust to changes in coding (genes vs. gene pairs, two-state vs. multistate, aligned vs. non-aligned), tree reconstruction methods, and the treatment of the two monogonont mt genomes. Thus, mt gene order verifies seisonids as sister to acanthocephalans within monophyletic Hemirotifera, while deviating results of sequence-based analyses reflect artificial signal. This conclusion implies that the complex life cycle of extant acanthocephalans evolved from a free-living state, as retained by most monogononts and bdelloids, via an epizoic state with a simple life cycle, as shown by seisonids. Hence, Acanthocephala represent a rare example where ancestral transitional stages have counterparts amongst the closest relatives., (Copyright © 2015 Elsevier Inc. All rights reserved.)

The taxon Syndermata comprises the biologically interesting wheel animals ("Rotifera": Bdelloidea + Monogononta + Seisonidea) and thorny-headed worms (Acanthocephala), and is central for testing superordinate phylogenetic hypotheses (Platyzoa, Gnathifera) in the metazoan tree of life. Recent analyses of syndermatan phylogeny suggested paraphyly of Eurotatoria (free-living bdelloids and monogononts) with respect to endoparasitic acanthocephalans. Data of epizoic seisonids, however, were absent, which may have affected the branching order within the syndermatan clade. Moreover, the position of Seisonidea within Syndermata should help in understanding the evolution of acanthocephalan endoparasitism. Here, we report the first phylogenomic analysis that includes all four higher-ranked groups of Syndermata. The analyzed data sets comprise new transcriptome data for Seison spec. (Seisonidea), Brachionus manjavacas (Monogononta), Adineta vaga (Bdelloidea), and Paratenuisentis ambiguus (Acanthocephala). Maximum likelihood and Bayesian trees for a total of 19 metazoan species were reconstructed from up to 410 functionally diverse proteins. The results unanimously place Monogononta basally within Syndermata, and Bdelloidea appear as the sister group to a clade comprising epizoic Seisonidea and endoparasitic Acanthocephala. Our results support monophyly of Syndermata, Hemirotifera (Bdelloidea + Seisonidea + Acanthocephala), and Pararotatoria (Seisonidea + Acanthocephala), rejecting monophyly of traditional Rotifera and Eurotatoria. This serves as an indication that early acanthocephalans lived epizoically or as ectoparasites on arthropods, before their complex lifecycle with arthropod intermediate and vertebrate definite hosts evolved.

The monophyletic origin of Spiralia within the metazoan tree of life is supported by many large-scale phylogenomic data. While there is now substantial molecular evidence for Lophotrochozoa being a monophyletic taxon within Spiralia, the phylogenetic affiliations of many other spiralian phyla remain unclear. Here we focus on the question of a monophyletic taxon Gnathifera, which was originally characterized by jaw morphology as comprising the taxa Rotifera, Acanthocephala and Gnathostomulida. Based on a large-scale molecular sequence dataset of 11,146 amino acid residues, we reconstructed phylogenetic trees of spiralian phyla using maximum-likelihood and Bayesian approaches. We obtain the first phylogenomic evidence for the clade Gnathifera, linking Syndermata (Rotifera+Acanthocephala) with Gnathostomulida. Furthermore, our data support recent findings concerning the paraphyly of Eurotatoria.