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Multiple evolutionary routes of the single polar capsule in Thelohanellus species (Myxozoa; Myxobolidae).

ABSTRACT: Thelohanellus Kudo, 1933 is a species rich genus of Myxosporea, sharing many morphological similarities with species of Myxobolus but the former possesses a single polar capsule, and the latter has two. Based on molecular phylogenetic analyses, this single distinguishing feature is not monophyletic, and members of Thelohanellus are intermixed with Myxobolus species, calling into question the validity of genus Thelohanellus. The occurrence of two polar capsules in a small proportion of Thelohanellus spores as observed in this study suggests that these species have the capacity to express this Myxobolus-like trait, clouding the distinction of these two genera further. Herein, using the most comprehensive data set to date, we explored the phylogenetic relationships of Thelohanellus to other myxobolids, to investigate the evolutionary history of the genus Thelohanellus and the origins of single polar capsule in this group. The phylogenetic analyses and statistical tests of topology revealed Thelohanellus as a strongly supported polyphyletic lineage, clustering in five distinct branches within Myxobolus clade. Ancestral state reconstruction for polar capsule number showed that Thelohanellus species have evolved from myxosporean species with two polar capsules at least four times, which could be classified in three possible evolutionary pathways. The polyphyly of Thelohanellus and the multiple evolutionary origins of single polar capsule of Thelohanellus demonstrate that the distinction of this genus from Myxobolus is largely for convenience, and does not reflect their evolutionary history.

SUBMITTER: Zhang X

PROVIDER: S-EPMC6319017 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Multiple evolutionary routes of the single polar capsule in Thelohanellus species (Myxozoa; Myxobolidae).

Zhang Xiuping X Liu Yang Y Whipps Christopher M CM Guo Qingxiang Q Gu Zemao Z

International journal for parasitology. Parasites and wildlife 20181129

Thelohanellus Kudo, 1933 is a species rich genus of Myxosporea, sharing many morphological similarities with species of Myxobolus but the former possesses a single polar capsule, and the latter has two. Based on molecular phylogenetic analyses, this single distinguishing feature is not monophyletic, and members of Thelohanellus are intermixed with Myxobolus species, calling into question the validity of genus Thelohanellus. The occurrence of two polar capsules ...[more]

PMID: 30622892

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Project description:BackgroundThe animal phylum Cnidaria consists of six classes or subphyla: Hydrozoa, Scyphozoa, Cubozoa, Staurozoa, Anthozoa, and Endocnidozoa. Cnidarians have an early evolutionary origin, diverging before the emergence of the Bilateria. Extant members from this phylum, therefore, are important resources for understanding the evolution of the nervous system. Cnidarian nervous systems are strongly peptidergic. Using genomics, we have recently shown that three neuropeptide families (the X1PRX2amides, GRFamides, and GLWamides) are wide-spread in four (Scyphozoa, Cubozoa, Staurozoa, Anthozoa) out of six cnidarian classes or subphyla, suggesting that these three neuropeptide families emerged in the common cnidarian ancestor. In the current paper, we analyze the remaining cnidarian class, Hydrozoa, and the subphylum Endocnidozoa, to make firm conclusions about the evolution of neuropeptide genes in Cnidaria.ResultsWe analyzed sixteen hydrozoan species with a sequenced genome or transcriptome, using a recently developed software program for discovering neuropeptide genes. These species belonged to various hydrozoan subclasses and orders, among them the laboratory models Hydra, Hydractinia, and Clytia. We found that each species contained three to five neuropeptide families. A common feature for all hydrozoans was that they contained genes coding for (i) X1PRX2amide peptides, (ii) GRFamide peptides, and (iii) GLWamide peptides. These results support our previous conclusions that these three neuropeptide families evolved early in evolution. In addition to these three neuropeptide families, hydrozoans expressed up to two other neuropeptide gene families, which, however, were only occurring in certain animal groups. Endocnidozoa (Myxozoa) are microscopically small endoparasites, which are strongly reduced. For long, it was unknown to which phylum these parasites belonged, but recently they have been associated with cnidarians. We analyzed nine endocnidozoan species and found that two of them (Polypodium hydriforme and Buddenbrockia plumatellae) expressed neuropeptide genes. These genes coded for neuropeptides belonging to the GRFamide and GLWamide families with structures closely resembling them from hydrozoans.ConclusionsWe found X1PRX2amide, GRFamide, and GLWamide peptides in all species belonging to the Hydrozoa, confirming that these peptides originated in the common cnidarian ancestor. In addition, we discovered GRFamide and GLWamide peptide genes in some members of the Endocnidozoa, thereby linking these parasites to Hydrozoa.

Dataset Information

Multiple evolutionary routes of the single polar capsule in Thelohanellus species (Myxozoa; Myxobolidae).

Publications

Multiple evolutionary routes of the single polar capsule in <i>Thelohanellus</i> species (Myxozoa; Myxobolidae).

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