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Whole-genome analyses converge to support the Hemirotifera hypothesis within Syndermata (Gnathifera)

  • ROTIFERA XVI
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Abstract

The clade Syndermata includes the endoparasitic Acanthocephala, the epibiotic Seisonidea, and the free-living Bdelloidea and Monogononta. The phylogeny of Syndermata is highly debated, hindering the understanding of the evolution of morphological features, reproductive modes, and lifestyles within the group. Here, we use publicly available whole-genome data to re-evaluate syndermatan phylogeny and assess the credibility of alternative hypotheses, using a new combination of phylogenomic methods. We found that the Hemirotifera and Pararotatoria hypotheses were recovered under combinations of datasets and methods with reduced possibility of systematic error in concatenation-based analyses. In contrast, the Seisonidea-sister and Lemniscea hypotheses were recovered under dataset combinations with increased possibility of systematic error. Hemirotifera was further supported by whole-genome microsynteny analyses and species-tree methods that use multi-copy orthogroups after removing distantly related outgroups. Pararotatoria was only partially supported by microsynteny-based phylogenomic reconstructions. Hence, Hemirotifera and partially Pararotatoria were supported by independent phylogenetic methods and data-evaluation approaches. These two hypotheses have important implications for the evolution of syndermatan morphological features, such as the gradual reduction of locomotory ciliation from the common ancestor of Syndermata in the stem lineage of Pararotatoria. Our study illustrates the importance of combining various types of evidence to resolve difficult phylogenetic questions.

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Data availability

The datasets supporting the conclusions of this article are available in the figshare digital repository (https://doi.org/10.6084/m9.figshare.22182697.v1). Custom bioinformatic scripts that were used for data processing are also provided on github (https://github.com/alexvasilikop/Rotifer_phylogeny).

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Acknowledgements

We thank all members of the Research Unit of Molecular Biology and Evolution (Université libre de Bruxelles, Belgium) and the participants of the XVI International Rotifer Symposium for the interesting and helpful discussions. This work was funded by the Philippe WIENER – Maurice ANSPACH Foundation through a collaborative project of KVD and TGB. This research was also supported by the grant agreement 725998 (RHEA) from the European Research Council (ERC CoG) to KVD, providing funding for AV. RWN, CGW, and TGB were funded by Natural Environment Research Council grants NE/M01651X/1 and NE/S010866/1. Financial support by the Deutsche Forschungsgemeinschaft (HE3487/5-1) to HH is gratefully acknowledged.

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Correspondence to Alexandros Vasilikopoulos or Karine Van Doninck.

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Handling editor: Sidinei M. Thomaz

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Guest editors: Maria Špoljar, Diego Fontaneto, Elizabeth J. Walsh & Natalia Kuczyńska-Kippen / Diverse Rotifers in Diverse Ecosystems

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Vasilikopoulos, A., Herlyn, H., Fontaneto, D. et al. Whole-genome analyses converge to support the Hemirotifera hypothesis within Syndermata (Gnathifera). Hydrobiologia 851, 2795–2826 (2024). https://doi.org/10.1007/s10750-023-05451-9

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  • DOI: https://doi.org/10.1007/s10750-023-05451-9

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