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New considerations on the phylogeny of Sessilida (Protista: Ciliophora: Peritrichia) based on multiple-gene information, with emphasis on colonial taxa

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Abstract

The subclass Peritrichia, containing two orders Sessilida and Mobilida, is a major group of ciliates with worldwide distribution and high species diversity. Several studies have investigated the phylogeny of peritrichs; however, the evolutionary relationships and classification of some families and genera within the Sessilida remain unclear. In the present study, we isolated and identified 22 peritrich populations representing four families and six genera and obtained 64 rDNA sequences to perform phylogenetic analyses and assess their systematic relationships. Ancestral character reconstruction was also carried out to infer evolutionary routes within the Sessilida. The results indicate: (1) family Vaginicolidae is monophyletic and acquisition of the typical peritrich lorica represents a single evolutionary divergence; (2) core epistylidids evolved from a Zoothamnium-like ancestor and experienced spasmoneme loss during evolution; (3) Campanella clusters with species in the basal clade and shows stable morphological differences with other epistylidids, supporting its assignment to a separate family; (4) the structure of the peristomial lip may be a genus-level character rather than a diagnostic character for discriminating Epistylididae and Operculariidae, thus a redefinition of Operculariidae should be carried out when more species have been investigated; (5) some characters, such as lifestyle (solitary or colonial), spasmoneme and living habit (sessile or free-swimming), evolved repeatedly among sessilids indicating that species with non-contractile stalks or that are free-swimming have multiple evolutionary routes and might derive from any sessilid lineage without a lorica. The close phylogenetic relationships of some morphologically distinct sessilids imply that the diagnoses of some genera and families should be improved.

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Data availability

Most datasets generated or analyzed during this study are included in this published article, and the rests are available from the corresponding author on reasonable request.

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Acknowledgements

Thanks are given to Prof. Weibo Song (Ocean University of China) for his constructive suggestions during the drafting of the manuscript. We thank Hao Yang from College of Fishery, Huazhong Agricultural University for his help in providing the sequences of Trichodina species. This work was supported by the Laoshan Laboratory (No. LSKJ202203201), the National Key Research and Development Program of China (2020YFD0900303), National Natural Science Foundation of China (project numbers: 32030015, 32000300, 32270481, 32100382), Hubei Agricultural Sciences and Technology Innovation Center (2021-620-000-001-33), China Postdoctoral Science Foundation Grant (project numbers: 2022M711922, 2021M701993) and the Researchers Supporting Project (Project number RSP2022R10) of King Saud University, Saudi Arabia. Our thanks are also given to the Weishan Wetland Station for institutional support.

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Authors and Affiliations

  1. Marine College, Shandong University, Weihai, 264209, China

    Zhe Wang, Lifang Li & Chundi Wang

  2. College of Fisheries/Shuangshui Shuanglü Institute, Huazhong Agricultural University, Wuhan, 430070, China

    Zhe Wang, Xiaoting Feng & Zemao Gu

  3. Hubei Engineering Technology Research Center for Aquatic Animal Diseases Control and Prevention, Wuhan, 430070, China

    Xiaoting Feng & Zemao Gu

  4. Department of Zoology, College of Science, King Saud University, Riyadh, 11451, Saudi Arabia

    Khaled A. S. Al-Rasheid

  5. Department of Life Sciences, Natural History Museum, London, SW7 5BD, UK

    Alan Warren

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Contributions

ZMG and CDW conceived and guided the study. ZW and XTF conducted the research; ZW and CDW wrote the manuscript; LFL, KASA and AW revised and edited the manuscript. All the authors read and approved the final version of the manuscript.

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Correspondence to Chundi Wang or Zemao Gu.

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The authors declare that they have no conflict of interest. Author Alan Warren is one of the Editorial Board Members, but he was not involved in the journal's review of, or decision related to, this manuscript.

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We declare that all applicable international, national, and or institutional guidelines for sampling, care, and experimental use of organisms for the study have been followed and all necessary approvals have been obtained.

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Edited by Jiamei Li.

Special topic: Ciliatology.

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Wang, Z., Feng, X., Li, L. et al. New considerations on the phylogeny of Sessilida (Protista: Ciliophora: Peritrichia) based on multiple-gene information, with emphasis on colonial taxa. Mar Life Sci Technol 4, 569–583 (2022). https://doi.org/10.1007/s42995-022-00155-w

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