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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Molecular phylogenetic position and description of a new genus and species of freshwater Chaetonotidae (Gastrotricha: Chaetonotida: Paucitubulatina), and the annotation of its mitochondrial genome

Leandro Gammuto A # , Valentina Serra A # , Giulio Petroni A B C and M. Antonio Todaro https://orcid.org/0000-0002-6353-7281 D E *
+ Author Affiliations
- Author Affiliations

A Dipartimento di Biologia, Università di Pisa, Pisa, Italy.

B Centro Interdipartimentale di Microscopia Elettronica (CIME), Università di Pisa, Pisa, Italy.

C Centro per l’Integrazione Della Strumentazione (CISUP), Università di Pisa, Pisa, Italy.

D Dipartimento di Scienze della Vita, Università di Modena e Reggio Emilia, Modena, Italy.

E National Biodiversity Future Center (NBFC), Palermo, Italy.

* Correspondence to: antonio.todaro@unimore.it
# These authors contributed equally to this paper

Handling Editor: Katrine Worsaae

Invertebrate Systematics 38, IS23059 https://doi.org/10.1071/IS23059
Submitted: 28 December 2023  Accepted: 19 June 2024  Published: 9 July 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

Chaetonotidae is the most diversified family of the entire phylum Gastrotricha; it comprises ~430 species distributed across 16 genera. The current classification, established mainly on morphological traits, has been challenged in recent years by phylogenetic studies, indicating that the cuticular ornamentations used to discriminate among species may be misleading when used to identify groupings, which has been the practice until now. Therefore, a consensus is developing toward implementing novel approaches to better define species identity and affiliation at a higher taxonomic ranking. Using an integrative morphological and molecular approach, including annotation of the mitogenome, we report on some freshwater gastrotrichs characterised by a mixture of two types of cuticular scales diagnostic of the genera Aspidiophorus and Heterolepidoderma. Our specimens’ overall anatomical characteristics find no correspondence in the taxa of these two genera, calling for their affiliation to a new species. Phylogenetic analyses based on the sequence of the ribosomal RNA genes of 96 taxa consistently found the new species unrelated to Aspidiophorus or Heterolepidoderma but allied with Chaetonotus aff. subtilis, as a subset of a larger clade, including mostly planktonic species. Morphological uniqueness and position along the non-monophyletic Chaetonotidae branch advocate erecting a new genus to accommodate the current specimens; consequently, the name Litigonotus ghinii gen. nov., sp. nov. is proposed. The complete mitochondrial genome of the new taxon resulted in a single circular molecule 14,384 bp long, including 13 protein-coding genes, 17 tRNA genes and 2 rRNAs genes, showing a perfect synteny and collinearity with the only other gastrotrich mitogenome available, a possible hint of a high level of conservation in the mitochondria of Chaetonotidae.

ZooBank: urn:lsid:zoobank.org:pub:9803F659-306F-4EC3-A73B-8C704069F24A

Keywords: biodiversity, fresh water, gastrotrichs, hairy-bellied worms, meiofauna, mitogenome, phylogeny, systematics, taxonomy.

References

Arias-Carrasco R, Vásquez-Morán Y, Nakaya HI, Maracaja-Coutinho V (2018) StructRNAfinder: an automated pipeline and web server for RNA families prediction. BMC Bioinformatics 19, 55.
| Crossref | Google Scholar | PubMed |

Balsamo M (1983) Three new gastrotrichs from a Tuscan–Emilian Apennine lake. Bolletino di Zoologia 49(3–4), 287-295 [1982 volume, published 17 May 1983].
| Crossref | Google Scholar |

Balsamo M, Grilli P, Guidi L, d’Hondt JL (2014) Gastrotricha – biology, ecology and systematics. Families Dasydytidae, Dichaeturidae, Neogosseidae, Proichthydiidae. In ‘Identification guides to the plankton and benthos of inland waters. Vol 24’. (Ed. HJF Bumont) pp. 1–187. (Backhuys Publishers: Weikersheim, Germany)

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Pyshkin AV (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology 19, 455-477.
| Crossref | Google Scholar | PubMed |

Bekkouche N, Worsaae K (2016) Neuromuscular study of early branching Diuronotus aspetos (Paucitubulatina) yields insights into the evolution of organs systems in Gastrotricha. Zoological Letters 2, 21.
| Crossref | Google Scholar | PubMed |

Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: Improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution 69, 313-319.
| Crossref | Google Scholar | PubMed |

Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9(8), 772.
| Crossref | Google Scholar |

Garraffoni ARS, Melchior RP (2015) New species and new records of freshwater Heterolepidoderma (Gastrotricha: Chaetonotidae) from Brazil with an identification key to the genus. Zootaxa 4057, 551-568.
| Crossref | Google Scholar | PubMed |

Garraffoni ARS, Araújo TQ, Lourenço AP, Guidi L, Balsamo M (2017) A new genus and new species of freshwater Chaetonotidae (Gastrotricha: Chaetonotida) from Brazil with phylogenetic position inferred from nuclear and mitochondrial DNA sequences. Systematics and Biodiversity 15, 49-62.
| Crossref | Google Scholar |

Golombek A, Tobergte S, Struck TH (2015) Elucidating the phylogenetic position of Gnathostomulida and first mitochondrial genomes of Gnathostomulida, Gastrotricha and Polycladida (Platyhelminthes). Molecular Phylogenetics and Evolution 86, 49-63.
| Crossref | Google Scholar | PubMed |

Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696-704.
| Crossref | Google Scholar | PubMed |

Hochberg R, Litvaitis MK (2000) Phylogeny of Gastrotricha: a morphology-based framework of gastrotricha relationships. Biological Bulletin 198, 299-305.
| Crossref | Google Scholar | PubMed |

Hummon WD, Balsamo M, Todaro MA (1992) Italian marine Gastrotricha. I. Six new and one redescribed species of Chaetonotida. Bollettino di Zoologia 59, 499-516.
| Crossref | Google Scholar |

International Commission on Zoological Nomenclature (1999) ‘International code of zoological nomenclature’, 4th edn. (The International Trust for Zoological Nomenclature)

International Commission on Zoological Nomenclature (2017) Declaration 45 – addition of recommendations to article 73 and of the term “specimen, preserved” to the glossary. Bullettin of Zoological Nomenclature 73, 2-4.
| Crossref | Google Scholar |

Kånneby T, Todaro MA (2015) The phylogenetic position of Neogosseidae (Gastrotricha: Chaetonotida) and the origin of planktonic Gastrotricha. Organisms Diversity and Evolution 15, 459-469.
| Crossref | Google Scholar |

Kånneby T, Todaro MA (2017) A new species of Aspidiophorus (Gastrotricha: Chaetonotidae) from the Swedish west coast. Zootaxa 4290, 390-394.
| Crossref | Google Scholar |

Kånneby T, Todaro MA, Jondelius U (2009) One new species and records of Ichthydium Ehrenberg, 1830 (Gastrotricha: Chaetonotida) from Sweden with a key to the genus. Zootaxa 2278, 26-46.
| Crossref | Google Scholar |

Kånneby T, Todaro MA, Jondelius U (2013) Phylogeny of Chaetonotidae and other Paucitubulatina (Gastrotricha: Chaetonotida) and colonization of aquatic ecosystems. Zoologica Scripta 42, 88-105.
| Crossref | Google Scholar |

Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in bioinformatics 20, 1160-1166.
| Crossref | Google Scholar | PubMed |

Kieneke A, Schmidt-Rhaesa A (2015) Gastrotricha. In ‘Handbook of Zoology: Gastrotricha, Cycloneuralia and Gnathifera. Vol. 3: Gastrotricha and Gnathifera’. (Ed. A Schmidt-Rhaesa) pp. 1–134. (De Gruyter)doi:10.1515/9783110274271

Kieneke A, Riemann O, Ahlrichs WH (2008) Novel implications for the basal internal relationships of Gastrotricha revealed by an analysis of morphological characters. Zoologica Scripta 37, 429-460.
| Crossref | Google Scholar |

Kolicka M, Kisielewski J, Nesteruk T, Zawierucha K (2013) Gastrotricha from the Poznan Palm House – one new subgenus and three new species of freshwater Chaetonotida (Gastrotricha). Zootaxa 3717, 231-279.
| Crossref | Google Scholar | PubMed |

Kolicka M, Dabert M, Dabert J, Kånneby T, Kisielewski J (2016) Bifidochaetus, a new Arctic genus of freshwater Chaetonotida (Gastrotricha) from Spitsbergen revealed by an integrative taxonomic approach. Invertebrate Systematics 30, 398-419.
| Crossref | Google Scholar |

Kolicka M, Dabert M, Olszanowski Z, Dabert J (2020) Sweet or salty? The origin of freshwater gastrotrichs (Gastrotricha, Chaetonotida) revealed by molecular phylogenetic analysis. Cladistics 36, 458-480.
| Crossref | Google Scholar |

Leasi F, Todaro MA (2008) The muscular system of Musellifer delamarei (Renaud-Mornant, 1968) and other chaetonotidans with implications for the phylogeny and systematisation of the Paucitubulatina (Gastrotricha). The Biological Journal of the Linnean Society 94, 379-398.
| Crossref | Google Scholar |

López-López A, Vogler AP (2017) The mitogenome phylogeny of Adephaga (Coleoptera). Molecular Phylogenetics and Evolution 114, 166-174.
| Crossref | Google Scholar | PubMed |

Monnens M, Thijs S, Briscoe AG, Clark M, Frost EJ, Littlewood DTJ, et al. (2020) The first mitochondrial genomes of endosymbiotic rhabdocoels illustrate evolutionary relaxation of atp8 and genome plasticity in flatworms. International Journal of Biological Macromolecules 162, 454-469.
| Crossref | Google Scholar | PubMed |

Poliseno A, Feregrino C, Sartoretto S, Aurelle D, Wörheide G, McFadden CS, Vargas S (2017) Comparative mitogenomics, phylogeny and evolutionary history of Leptogorgia (Gorgoniidae). Molecular Phylogenetics and Evolution 115, 181-189.
| Crossref | Google Scholar | PubMed |

Rataj Križanová F, Vďačný P (2024) A Heterolepidoderma and Halichaetoderma gen. nov. (Gastrotricha: Chaetonotidae) riddle: integrative taxonomy and phylogeny of six new freshwater species from central Europe. Zoological Journal of the Linnean Society 200(2), 283-335.
| Crossref | Google Scholar |

Remane A (1925) Organisation und systematische Stellung der aberranten Gastrotrichen. Verhandlungen der Deutschen Zoologische Gesellschaft 30, 121-128 [In German].
| Google Scholar |

Remane A (1927) Gastrotricha. In ‘Die Tierwelt der Nord- und Ostsee’. (Ed. G Grimpe). pp. 1–56. (Akademische Verlagsgesellschaft: Leipzig, German Republic) [In German]

Remane A (1936) Gastrotricha. In ‘Klassen Ordnungen des Tierreichs, Band 4, Abteilung II, Buch I, Teil 2, Liefrungen 1-2’. (Ed. HG Bronns). pp. 1–242. (Akademie Verlagsgesellschaft: Berlin, German Republic) [In German]

Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Huelsenbeck (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539-542.
| Crossref | Google Scholar | PubMed |

Saponi F, Todaro MA (2024) Status of the Italian freshwater Gastrotricha biodiversity, with the creation of an interactive GIS-based web map. Diversity 16, 17.
| Crossref | Google Scholar |

Saponi F, Kosakyan A, Cesaretti A, Todaro MA (2024) How anthropogenic actions affect gastrotrichs diversity in Italian freshwaters. In ‘Symposium: Cambiamento della biodiversità nell’Antropocene: priorità per la Ricerca’, 10–11 April 2024, Fano, Italy. Poster presentation 62. (Consiglio Nazionale delle Ricerche, CNR: Rome, Italy) Available at https://drive.google.com/drive/folders/1gEZWs2B-mRQ1jkm8b_hyrft4k66nSYt5

Saponi F, Kosakyan A, Cesaretti A, Todaro MA (in press) A contribution to the taxonomy and phylogeny of the genus Chaetonotus (Gastrotricha, Paucitubulatina, Chaetonotidae), with the description of a new species from Italian inland waters. European Zoological Journal .
| Google Scholar |

Schwank P (1990) Gastrotricha. In ‘Susswasserfauna von Mitteleuropa’. (Eds J Schwoerbel, P Zwick) pp. 1–252. (Gustav Fisher Verlag: Stuttgart, Germany) [In German]

Timmermans MJ, Lees DC, Simonsen TJ (2014) Towards a mitogenomic phylogeny of Lepidoptera. Molecular Phylogenetics and Evolution 79, 169-178.
| Crossref | Google Scholar | PubMed |

Todaro MA, d’Hondt J-L (2023) Gastrotricha. In ‘WoRMS: World Register of Marine Species’. (Flanders Marine Institute) Available at https://www.marinespecies.org/aphia.php?p=taxdetails&id=2078

Todaro MA, Perissinotto R, Bownes SJ (2013) Neogosseidae (Gastrotricha, Chaetonotida) from the iSimangaliso Wetland Park, KwaZulu–Natal, South Africa. Zookeys 315, 77-94.
| Crossref | Google Scholar | PubMed |

Todaro MA, Sibaja-Cordero JA, Segura-Bermúdez OA, Coto-Delgado G, Goebel-Otarola N, et al. (2019) An introduction to the study of Gastrotricha, with a taxonomic key to families and genera of the group. Diversity 11, e117.
| Crossref | Google Scholar |

Voigt M (1902) Diagnosen bisher unbeschreibener Organismen aus Piöner Gewässern. Die Rotatorien und Gastrotrichen Der Umbbung von Ploen. Zoologisher Anzeiger 25, 35-39 [In German].
| Google Scholar |

Westram R, Bader K, Pruesse E, Kumar Y, Meier H, Glöckner FO, Ludwig W (2011) ARB: a software environment for sequence data. In ‘Handbook of Molecular Microbial Ecology I: Metagenomics and Complementary Approaches’. (Ed. FJ Bruijn) pp. 399–406. (Wiley–Blackwell Publishing) 10.1002/9781118010518.ch46