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Hypotrichidium tisiae (Gelei, 1929) Gelei, 1954: a unique hypotrichid ciliate having a highly specialized developmental pattern during binary division

Marine Life Science & Technology volume 4, pages 536–550 (2022)Cite this article

Abstract

In sharp contrast to their pelagic relatives, the oligotrichs, the overwhelming majority of hypotrich ciliates inhabit the benthos. Only a few species, including those of the genus Hypotrichidium Ilowaisky, 1921, have adapted to a planktonic lifestyle. The ontogenetic mode of the highly differentiated ciliate, Hypotrichidium tisiae (Gelei, 1929) Gelei, 1954, is unknown. In this study, the interphase morphology and the ontogenetic process of this species are investigated. Accordingly, the previously unidentified ciliary pattern of Hypotrichidium is redefined. The main morphogenetic features are as follows: (1) The parental adoral zone of membranelles is inherited completely by the proter and the oral primordium of the opisthe arises in a deep pouch. (2) Five frontoventral cirral anlagen (FVA) are formed: FVA I contributes to the single frontal cirrus, FVA II–IV generate three frontoventral cirral rows, FVA V migrates and forms postoral ventral cirri. (3) All marginal cirral row anlagen develop de novo: each of the two left anlagen forms a single cirral row, while the single right anlage fragments into anterior and posterior parts. (4) Two dorsal kinety anlagen occur de novo, with the right one fragmenting to form kineties 2 and 3. (5) Two long caudal cirral rows are formed at the ends of dorsal kineties 1 and 3. On the basis of the morphogenetic features and phylogenetic analyses, the assignment of Hypotrichidium to the family Spirofilidae Gelei, 1929 within Postoralida is supported. The establishment of separate families for the slender “tubicolous” spirofilids and the highly helical spirofilids is also validated.

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Data availability

The small subunit ribosomal RNA gene sequences generated during the present study have been deposited to GenBank with accession number: ON117314–ON117316 (https://www.ncbi.nlm.nih.gov/nuccore). The other data generated or analyzed during this study are included in this manuscript and supporting files.

References

  • Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, Agatha S, Berney C, Brown MW, Burki F, Cárdenas P, Čepička I, Chistyakova L, del Campo J, Dunthorn M, Edvardsen B, Eglit Y, Guillou L, Hampl V, Heiss AA et al (2019) Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol 66:4–119

    Article  PubMed  PubMed Central  Google Scholar 

  • Alfaro M (2003) Bayes or bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol Biol Evol 20:255–266

    Article  CAS  PubMed  Google Scholar 

  • Bai Y, Wang R, Song W, Suzuki T, Hu X (2020) Redescription of five tintinnine ciliates (Alveolata: Ciliophora: Oligotrichea) from coastal waters of Qingdao, China. Mar Life Sci Technol 2:209–221

    Article  Google Scholar 

  • Berger H (1999) Monograph of the Oxytrichidae (Ciliophora, Hypotrichia). Monographiae Biol 78:1–1080

    Article  Google Scholar 

  • Berger H (2006) Monograph of the Urostyloidea (Ciliophora, Hypotricha). Monographiae Biol 85:1–1304

    Article  Google Scholar 

  • Berger H (2008) Monograph of the Amphisiellidae and Trachelostylidae (Ciliophora, Hypotricha). Monographiae Biol 88:1–737

    Google Scholar 

  • Berger H (2011) Monograph of the Gonostomatidae and Kahliellidae (Ciliophora, Hypotricha). Monographiae Biol 90:1–741

    Article  Google Scholar 

  • Borror AC (1972) Revision of the order Hypotrichida (Ciliophora, Protozoa). J Protozool 19:1–23

    Article  CAS  PubMed  Google Scholar 

  • Bourland WA (2015) Morphology, ontogenesis and molecular characterization of Atractos contortus Vörösváry, 1950 and Stichotricha aculeata Wrzesniowskiego, 1866 (Ciliophora, Stichotrichida) with consideration of their systematic positions. Eur J Protistol 51:351–373

    Article  PubMed  Google Scholar 

  • Chen L, Liu W, Liu A, Al-Rasheid KAS, Shao C (2013) Morphology and molecular phylogeny of a new marine hypotrichous ciliate, Hypotrichidium paraconicum n. sp. (Ciliophora, Hypotrichia). J Eukaryot Microbiol 60:588–600

    Article  PubMed  Google Scholar 

  • Chen L, Zhao X, Ma H, Warren A, Shao C, Huang J (2015) Morphology, morphogenesis and molecular phylogeny of a soil ciliate, Pseudouroleptus caudatus caudatus Hemberger, 1985 (Ciliophora, Hypotricha), from Lhalu Wetland, Tibet. Eur J Protistol 51:1–14

    Article  PubMed  Google Scholar 

  • Chen X, Lu X, Luo X, Jiang J, Shao C, Al-Rasheid KAS, Warren A, Song W (2017) The diverse morphogenetic patterns in spirotrichs and philasterids researches based on five-year-projects supported by IRCN-BC and NSFC. Eur J Protistol 61:439–452

    Article  PubMed  Google Scholar 

  • Chen L, Liu Y, Long Y, Lyu J, Feng C, Ning Y, Yi Z (2021) Morphology and molecular phylogeny of two new soil ciliates, Hemiurosomoida warreni nov. spec. and Hemiurosoma clampi nov. spec. (Ciliophora, Hypotrichia) from Tibet. Eur J Protistol 77:125746

    Article  PubMed  Google Scholar 

  • Corliss JO (1961) The ciliated protozoa: characterization, classification, and guide to the literature. In: Kerkut GA (ed) International series of monographs on pure and applied biology, vol 7. Pergamon Press, Oxford, London, New York, Paris

    Google Scholar 

  • Corliss JO (1979) The ciliated protozoa. Characterization, classification and guide to the literature. Pergamon Press, Oxford, New York, Toronto, Sydney, Paris, Frankfurt

    Google Scholar 

  • Dingfelder JH (1962) Die Ciliaten vorübergehender Gewässer. Arch Protistenk 105:509–658

    Google Scholar 

  • Dragesco J, Dragesco-Kernéis A (1986) Ciliés libres de l’Afrique intertropicale. Introduction à la connaissance et à l’étude des ciliés. Faune Trop 26:1–559

    Google Scholar 

  • Fauré-Fremiet E (1961) Remarques sur la morphologie compare et la systématique des ciliata Hypotrichida. Acad Sci 252:3515–3519

    Google Scholar 

  • Foissner W (2016) Terrestrial and semiterrestrial ciliates (Protozoa, Ciliophora) from Venezuela and Galápagos. Denisia 35:1–912

    Google Scholar 

  • Foissner W, Stoeck T (2008) Morphology, ontogenesis and molecular phylogeny of Neokeronopsis (Afrokeronopsis) aurea nov. subgen. nov. spec. (Ciliophora: Hypotricha), a new African flagship ciliate confirms the CEUU hypothesis. Acta Protozool 47:1–33

    PubMed  PubMed Central  Google Scholar 

  • Foissner W, Shi X, Wang R, Warren A (2010) A reinvestigation of Neokeronopsis populations, including the description of N. asiatica nov. spec. (Ciliophora, Hypotricha). Acta Protozool 49:87–105

    Google Scholar 

  • Gao F, Warren A, Zhang Q, Gong J, Miao M, Sun P, Xu D, Huang J, Yi Z, Song W (2016) The all-data-based evolutionary hypothesis of ciliated protists with a revised classification of the phylum Ciliophora (Eukaryota, Alveolata). Sci Rep 6:24874

    Article  PubMed  PubMed Central  Google Scholar 

  • Gelei J (1929) Ein neuer Typ der hypotrichen Infusorien aus der Umgebung von Szeged. Spirofilum tisiae n. sp., n. gen., n. fam. Arch Protistenk 65:165–182

    Google Scholar 

  • Gelei J (1954) Über die Lebensgemeinschaft einiger temporärer Tümpel auf einer Bergwiese im Börzsönygebirge (Oberungarn) III. Ciliaten Acta Biol Hung 5:259–343

    Google Scholar 

  • Hausmann K, Bradbury PC (1996) Ciliates: cells as organisms. Gustav Fischer, Stuttgart

    Google Scholar 

  • Heber D, Stoeck T, Foissner W (2014) Morphology and ontogenesis of Psilotrichides hawaiiensis nov. gen., nov. spec. and molecular phylogeny of the Psilotrichidae (Ciliophora, Hypotrichia). J Eukaryot Microbiol 61:260–277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hemberger H (1985) Neue Gattungen und Arten hypotricher Ciliaten. Arch Protistenk 130:397–417

    Article  Google Scholar 

  • Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192

    Article  Google Scholar 

  • Hu X, Lin X, Song W (2019) Ciliate atlas: species found in the South China Sea. Science Press, Beijing

    Google Scholar 

  • Ilowaisky SA (1921) Zwei neue Arten und Gattungen von Infusorien aus dem Wolgabassin. Arb Biol Wolga Stat 6:103–106

    Google Scholar 

  • Jankowski AW (1975) A conspectus of the new system of subphylum Ciliophora Doflein, 1901. In: Balashov US (ed) Account of scientific sessions on results of scientific work, year 1974: abstracts of reports. Zool Inst Akad Nauk SSSR, Leningrad, pp 26–27

    Google Scholar 

  • Jankowski AW (1979) Revision of the order Hypotrichida Stein, 1859. Generic catalogue, phylogeny, taxonomy. Trudy Zool Inst Akad Nauk SSSR 86:46–85

    Google Scholar 

  • Jankowski AW (2007) Phylum Ciliophora Doflein, 1901. In: Alimov AF (ed) Protista. Part 2. Handbook on zoology. Russian Academy of Sciences, Zoological Institute, St. Petersburg, pp 415–993

    Google Scholar 

  • Jin D, Li L, Lyu J, Warren A, Shao C (2022) Morphogenesis and molecular phylogeny of a freshwater ciliate, Oxytricha multilineata n. sp. (Ciliophora, Hypotrichia). Eur J Protistol 82:125864

    Article  PubMed  Google Scholar 

  • Jung JH, Park KM, Min GS (2015) Morphology and molecular phylogeny of Pseudocyrtohymena koreana n. g. n. sp. and Antarctic Neokeronopsis asiatica Foissner et al. 2010 (Ciliophora, Sporadotrichida), with a brief discussion of the Cyrtohymena undulating membranes pattern. J Eukaryot Microbiol 62:280–297

    Article  CAS  PubMed  Google Scholar 

  • Jung JH, Omar A, Park MH, Nguyen TV, Jung YH, Yang HM, Min GS (2021) Anteholosticha foissneri n. sp., a marine hypotrich ciliate (Ciliophora: Spirotrichea) from Vietnam: morphology, morphogenesis, and molecular phylogeny. Eur J Protistol 78:125768

    Article  PubMed  Google Scholar 

  • Kahl A (1932) Urtiere oder Protozoa I: Wimpertiere oder Ciliata (Infusoria) 3. Spirotricha Tierwelt Dtl 25:399–650

    Google Scholar 

  • Kim JH, Vďačný P, Shazib SUA, Shin MK (2014) Morphology and molecular phylogeny of Apoterritricha lutea n. g., n. sp. (Ciliophora, Spirotrichea, Hypotrichia): a putative missing link connecting Cyrtohymena and Afrokeronopsis. J Eukaryot Microbiol 61:520–536

    Article  CAS  PubMed  Google Scholar 

  • Kim KS, Jung JH, Min GS (2019) Morphology and molecular phylogeny of two new terrestrial ciliates, Australocirrus rubrus n. sp. and Notohymena gangwonensis n. sp. (Ciliophora: Oxytrichidae), from south Korea. J Eukaryot Microbiol 66:740–751

    Article  PubMed  Google Scholar 

  • Kumar S, Foissner W (2015) Biogeographic specializations of two large hypotrich ciliates: Australocirrus shii and A. australis and proposed synonymy of Australocirrus and Cyrtohymenides. Eur J Protistol 51:210–228

    Article  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Li L, Wang J, Zhu E, Shao C (2021) Morphology, morphogenesis and molecular phylogeny of a novel soil ciliate, Afrokahliella paramacrostoma n. sp. (Ciliophora, Hypotrichia). Eur J Protistol 77:125748

    Article  PubMed  Google Scholar 

  • Liu W, Shin MK, Yi Z, Tan Y (2021) Progress in studies on the diversity and distribution of planktonic ciliates (Protista, Ciliophora) in the South China Sea. Mar Life Sci Technol 3:28–43

    Article  CAS  Google Scholar 

  • Luo X, Yan Y, Shao C, Al-Farraj SA, Bourland WA, Song W (2018) Morphological, ontogenetic, and molecular data support strongylidiids as being closely related to Dorsomarginalia (Protozoa, Ciliophora) and reactivation of the family Strongylidiidae Fauré-Fremiet, 1961. Zool J Linn Soc 184:237–254

    Article  Google Scholar 

  • Luo X, Bourland WA, Song W, Huang J (2021) New contributions to the taxonomy of urostylid ciliates (Ciliophora, Hypotrichia), with establishment of a new genus and new species. Eur J Protistol 80:125810

    Article  PubMed  Google Scholar 

  • Lynn DH (2008) The ciliated Protozoa: characterization, classification, and guide to the literature, 3rd edn. Springer Press, New York

    Google Scholar 

  • Lynn DH, Small EB (2002) Phylum Ciliophora. In: Lee JJ, Leedale GF, Bradbury P (eds) An illustrated guide to the Protozoa, 2nd edn. Organisms traditionally referred to as Protozoa, or newly discovered groups, vol I. Society of Protozoologists, Lawrence, pp 371–656

    Google Scholar 

  • Ma J, Zhang T, Song W, Shao C (2021a) New contributions to the diversity of hypotrichous ciliates: description of a new genus and two new species (Protozoa, Ciliophora, Hypotrichia). Front Microbiol 12:712269

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma J, Zhao Y, Zhang T, Shao C, Al-Rasheid KAS, Song W (2021b) Cell-division pattern and phylogenetic analyses of a new ciliate genus Parasincirra n. g. (Protista, Ciliophora, Hypotrichia), with a report of a new soil species, P. sinica n. sp. from northwest China. BMC Ecol Evol 21:21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao W, Song L, Ba S, Zhang L, Guan G, Zhang Z, Ning K (2020) Protist 10,000 genomes project. Innovation 1:100058

    PubMed  PubMed Central  Google Scholar 

  • Omar A, Moon JH, Jung JH (2021) Molecular phylogeny of a new gonostomatid ciliate revealing a discrepancy between interphasic and cell divisional patterns (Ciliophora, Hypotricha). Eur J Protistol 2021:125794

    Article  Google Scholar 

  • Omar A, Yeo JH, Jung JH (2022) A new “flagship” ciliate, Pseudostylonychia obliquocaudata n. gen., n. sp. (Ciliophora, Hypotricha), from South Korea. Eur J Protistol 84:125893

    Article  PubMed  Google Scholar 

  • Paiva TS (2020) Systematic redefinition of the Hypotricha (Alveolata, Ciliophora) based on combined analyses of morphological and molecular characters. Protist 171:125755

    Article  Google Scholar 

  • Rossolimo L (1930) Über Spirofilum tisiae Gelei und Hypotrichidium conicum Ilowaisky. Zool Anz 86:69–74

    Google Scholar 

  • Shao C, Chen X, Jiang J (2020) Hypotrichous ciliates in China. Science Press, Beijing

    Google Scholar 

  • Song WY, Luo X, Chi Y, Al-Farraj SA, Shao C (2022) Ontogenesis and systematic position of a new hypotrichous ciliate, Chaetospira sinica sp. nov, with an improved diagnosis of the poorly defined family Chaetospiridae Jankowski (Protozoa, Ciliophora, Hypotrichia) Mar Life Sci Technol. https://doi.org/10.1007/s42995-022-00146-x

  • Song WB, Shao C (2017) Ontogenetic patterns of hypotrich ciliates. Science Press, Beijing

    Google Scholar 

  • Song WB, Warren A, Hu X (2009) Free-living ciliates in the Bohai and Yellow Seas. Science Press, Beijing

    Google Scholar 

  • Stiller J (1975) Die familie Strongylidiidae Fauré-Fremiet, 1961 (Ciliata: Hypotrichida) und Revision der Gattung Hypotrichidium Ilowaisky, 1921. Acta Zool Hung 21:221–231

    Google Scholar 

  • Tuffrau M (1972) Caractères primitifs et structures évoluées chez les Ciliés hypotriches: le genre Hypotrichidium. Protistologica 8:257–266

    Google Scholar 

  • Tuffrau M (1987) Proposition d’une classification nouvelle de l’ordre Hypotrichida (Protozoa, Ciliophora), fondées récentes. Ann Sci Nat (zool) 13:111–117

    Google Scholar 

  • Tuffrau M, Fleury A (1994) Classe des Hypotrichea Stein, 1859. In: De Puytorac P (ed) Traité de Zoologie, Infusoires Ciliés, vol 2. Masson, Paris, pp 83–151

    Google Scholar 

  • Vďačný P, Foissner W (2021) Morphology and ontogenesis of two new Hemiholosticha species (Ciliophora, Hypotrichia, Hemiholostichidae nov. fam.). Eur J Protistol 77:125763

    Article  PubMed  Google Scholar 

  • Wang J, Zhang T, Li F, Warren A, Li Y, Shao C (2021a) A new hypotrich ciliate, Oxytricha xianica sp. nov., with notes on the morphology and phylogeny of a Chinese population of Oxytricha auripunctata Blatterer & Foissner, 1988 (Ciliophora, Oxytrichidae). Mar Life Sci Technol 3:303–312

    Article  CAS  Google Scholar 

  • Wang J, Zhao Y, Lu X, Lyu Z, Warren A, Shao C (2021b) Does the Gonostomum-patterned oral apparatus in Hypotrichia carry a phylogenetic signal? Evidence from morphological and molecular data based on extended taxon sampling using three nuclear genes (Ciliophora, Spirotrichea). Sci China Life Sci 64:311–322

    Article  CAS  PubMed  Google Scholar 

  • Wilbert N (1975) Eine verbesserte Technik der Protargolimprägnation für Ciliaten. Mikrokosmos 64:171–179

    Google Scholar 

  • Xu K, Lei Y (2007) A new spirofilid ciliate from the Yellow Sea: Metastrongylidium distichum n. gen., n. sp. (Ciliophora, Stichotrichia). Acta Protozool 46:121–129

    Google Scholar 

  • Xu W, Wang Y, Cheng T, Yu Y, El-Serehy H, Al-Farraj SA, Bourland WA, Luo X (2020) Reevaluation of the ‘well-known’ Paraurostyla weissei complex, with notes on the ontogenesis of a new Paraurostyla species (Ciliophora, Hypotrichia). Eur J Protistol 73:125672

    Article  PubMed  Google Scholar 

  • Xu W, Ma J, Bourland WA, Petroni G, Luo X, Song W (2022) Phylogeny of a new ciliate family Clampidae fam. nov. (Protista, Ciliophora), with notes on morphology and morphogenesis. Zool J Linn Soc 196:88–104

    Article  Google Scholar 

  • Zhang T, Dong J, Cheng T, Duan L, Shao C (2020) Reconsideration of the taxonomy of the marine ciliate Neobakuella aenigmatica Moon et al., 2019 (Protozoa, Ciliophora, Hypotrichia). Mar Life Sci Technol 2:97–108

    Article  Google Scholar 

  • Zhang T, Shao C, Zhang T, Song W, Vďačný P, Al-Farraj SA, Wang Y (2022) Multi-gene phylogeny of the ciliate genus Trachelostyla (Ciliophora, Hypotrichia), with integrative description of two species, Trachelostyla multinucleata spec. nov. and T. pediculiformis (Cohn, 1866). Front Microbiol 12:775570

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (Nos. 31900319, 32030015, 32070432), the National Key Research and Development Program of China (No. 2018YFD0900701), and the Youth Innovation Promotion Association of the Chinese Academy of Sciences (No. 2019333). We thank Prof. Xiaozhong Hu, Ocean University of China (OUC), for his helpful suggestions regarding species identification, and Prof. Weibo Song, OUC, for his comments on the manuscript.

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Authors and Affiliations

  1. Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, China

    Xiaotian Luo & Jie Huang

  2. Institute of Evolution and Marine Biodiversity & Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, 266003, China

    Honggang Ma & Yujie Liu

  3. Department of Biology, Shenzhen MSU-BIT University, Shenzhen, 518172, China

    Xiaoteng Lu

  4. Department of Zoology, Faculty of Science, Charles University, Prague, 12843, Czech Republic

    William A. Bourland

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Contributions

W.A.B: conceived and guided the study. X.Luo: collected samples and carried out the laboratory work. X.Lu: was responsible for the molecular phylogenetic analyses. X.Luo: drafted the manuscript. J.H, H.M, Y.L, X.Lu, and W.A.B: made further revisions. All authors read and approved the final version of manuscript

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Correspondence to Xiaoteng Lu or William A. Bourland.

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Special topic: Ciliatology.

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42995_2022_148_MOESM1_ESM.doc

Supplementary file1 Supplementary Fig. S1 A–L Photomicrographs showing interphase (A) and morphogenetic stages (B–J) of Hypotrichidium tisiae after protargol staining. A Ventral view of a typical specimen, showing infraciliature, arrowhead shows the single frontal cirrus, arrow indicates the acutely pointed tail. B Details of a very early divider, showing the replication bands of the macronuclear nodules (arrows), arrowheads mark the micronuclei. C Oral primordium of the opisthe. D Ventral view of an early divider, showing the V-shaped frontoventral cirral anlage and the right marginal cirral row anlage. E Ventral view of an early-middle divider, showing the elongated frontoventral cirral anlagen and the left marginal cirral row anlagen. F Details of an early-middle divider, showing five streak-like frontoventral cirral anlagen in the opisthe, arrow indicates the newly formed adoral membranelles. G The oral primordium located in the deep pouch (arrowhead) and the micronucleus. H Ventral view of a middle divider, showing new cirri formed from cirral anlagen, arrowhead indicates the newly formed frontal cirrus. I Dorsal view of a middle divider, showing dorsal kinety anlagen and caudal cirral row analgen. J Dorsal view of a middle-late divider, arrowhead shows the gap between anterior and posterior parts of the right marginal cirral row, arrows indicate caudal cirral row 2 fragmented from the end of dorsal kinety 3. ARMR new anterior part of right marginal cirral row, CC1, 2A caudal cirral row anlage, DK2, 3 new dorsal kineties, DK1–3A dorsal kinety anlagen, FVR1–3 new frontoventral cirral rows, LM1A left marginal cirral row 1 anlage, Mi micronuclei, OP oral primordium, PRMR new posterior part of right marginal cirral row, PVC new postoral ventral cirri, RMA right marginal cirral row anlage, I–V frontoventral cirral anlagen. Scale bar: 50 μm (DOC 2764 KB)

Supplementary file2 (DOC 93 KB)

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Luo, X., Huang, J., Ma, H. et al. Hypotrichidium tisiae (Gelei, 1929) Gelei, 1954: a unique hypotrichid ciliate having a highly specialized developmental pattern during binary division. Mar Life Sci Technol 4, 536–550 (2022). https://doi.org/10.1007/s42995-022-00148-9

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Keywords

  • Hypotrichs
  • Ontogenesis
  • Phylogeny
  • Spirofilidae
  • Systematics
  • 18S rRNA gene