Transcriptome Data Reveal Syndermatan Relationships and Suggest the Evolution of Endoparasitism in Acanthocephala via an Epizoic Stage

Abstract

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 complete mitochondrial genome sequence of Southwellina hispida supports monophyly of Palaeacanthocephala (Acanthocephala: Polymorphida)

“…Within Syndermata, phylogenetic trees recovered monophyly of Monogononta, Bdelloidea (rotifer groups), and Acanthocephala, each receiving very strong branch support. Paraphyly of Eurotatoria (Bdelloidea and Monogononta) was also observed in this study, as already confirmed in earlier studies [10,11,19,22,37]. The asexual rotifer group Bdelloidea was recovered as sister to Acanthocephala.…”

“…Analyses of a combined dataset including nuclear SSU and LSU rDNAs and mitochondrial cox1 sequences depicted Archiacanthocephala as the sister to a clade comprising all three other classes, in which Palaeacanthocephala was sister to Polyacanthocephala and Eoacanthocephala [9]. Other molecular analyses for the major acanthocephalan classes also showed similar results in that Archiacanthocephala is basal to the clade of Palaeacanthocephala and Eoacanthocephala (SSU) [19][20][21][22] and the most recent transcriptome data supported a sister relationship between Palaeacanthocephala and Eoacanthocephala [11]. Despite good resolution of acanthocephalan internal phylogeny either from morphology and/or from molecular data, palaeacanthocephalan monophyly has not always been supported.…”

“…Based on sharing some morphological characters including the eponymous syncytial epidermis and sperm ultrastructure, Acanthocephala and Rotifera (wheel animals) were combined as a clade Syndermata [3]. Their close relationship has also been supported by some other morphological evidence [4][5][6] and different types of molecular data (SSU rDNA [7,8]; SSU + LSU rDNAs and mitochondrial cox1 [9]; mitochondrial genome [10]; transcriptome data [11]). Acanthocephala was initially recognized as a subgroup of the Aschelminthes and included two orders: Palaeacanthocephala and Archiacanthocephala [12].…”

Gnathifera

“…Gnathifera has been placed in the Spiralia, often affi liated with the Platyzoa (Funch et al 2005 ;Dunn et al 2008 ;Witek et al 2008Witek et al , 2009Hejnol et al 2009 ;Wey-Fabrizius et al 2014 ). However, the sister group of Gnathifera remains unclear.…”

“…However, the sister group of Gnathifera remains unclear. Since gene sequences of most of the gnathiferan species seem to evolve fast, it remains diffi cult to resolve with confi dence the internal relationships using molecular data (Witek et al 2008 ;Wey-Fabrizius et al 2014 ). Figure 1.1 illustrates the likely phylogenetic relationships as a consensus phylogeny that is based on recent molecular as well as morphological data.…”