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The sperm of Xenacoelomorpha revisited: implications for the evolution of early bilaterians

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Abstract

Sperm structure of the Xenacoelomorpha (Acoelomorpha plus Xenoturbellida) is updated in the light of new discoveries or new interpretations of existing data. Nemertodermatida and Acoela (Acoelomorpha) have introsperm with certain basic features in common, but all acoels lack acrosomes and usually have two flagella with unusual combinations of microtubules, whereas all nemertodermatids have small, simple acrosomes and a typical 9 + 2 flagellum. Xenoturbellida is currently considered as the sister taxon to Acoelomorpha. Xenoturbella bocki has an aquasperm that has almost nothing in common with the sperm of Acoelomorpha. We argue that the aquasperm ultrastructure of X. bocki has much in common with sperm of hemichordates and to some extent echinoderms, which was previously disputed. Molecular analyses have on the one hand supported a connection with deuterostomes but on the other hand have negated it, suggesting that the closest common ancestor of Xenacoelomorpha is either the Nephrozoa, Deuterostomia or Protostomia. Sperm structure is highly diverse among Xenacoelomorpha, with protostome-like traits in Acoelomorpha and deuterostome-like traits in Xenoturbella. Assuming Xenacoelomorph monophyly and ancestral introsperm in this taxon, however, suggests that the re-expression of the aquasperm form of Xenoturbella, involving some key changes in sperm morphology, is a secondarily derived state that could have occurred through “progenetic spermiogenesis” with the precocious development of round spermatids to maturity.

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Acknowledgements

We are deeply indebted to the work of Seth Tyler, Reinhard Rieger and Jan Hendelberg for the original discovery of the nemertodermatid sperm in the 1970s. Seth Tyler kindly provided J.B-N. with grids that were used for further studies of the sperm of Flagellophora apelti and Andreas Hejnol supplied J.B-N. with fixed specimens of Convolutriloba longifissura and we thank them both very much. In memory of Jan Hendelberg and Reinhard Rieger.

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Authors and Affiliations

  1. Biology Department, St Francis Xavier University, Box 5000, Antigonish, NS, B2G2W5, Canada

    John Buckland-Nicks

  2. Gothenburg Natural History Museum, Box 7283, 40283, Gothenburg, Sweden

    Kennet Lundin

  3. Gothenburg Global Biodiversity Centre, Box 461, 40530, Gothenburg, Sweden

    Kennet Lundin

  4. Department of Medical Biochemistry and Microbiology, Science for Life Laboratory, Uppsala University, Uppsala, Sweden

    Andreas Wallberg

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  1. John Buckland-Nicks
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  2. Kennet Lundin
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  3. Andreas Wallberg
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Correspondence to John Buckland-Nicks.

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This study was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant (#46205) to John Buckland-Nicks.

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This study does not contain studies with human participants performed by any of the authors. All applicable international, national and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies using animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. All appropriate data created by the authors (i.e., photographs, diagrams) are available in the manuscript.

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Buckland-Nicks, J., Lundin, K. & Wallberg, A. The sperm of Xenacoelomorpha revisited: implications for the evolution of early bilaterians. Zoomorphology 138, 13–27 (2019). https://doi.org/10.1007/s00435-018-0425-8

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