The sperm of Xenacoelomorpha revisited: implications for the evolution of early bilaterians
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.
KeywordsSpermatozoa Ultrastructure Nemertodermatida Acoela Xenoturbella Phylogeny Bilateria
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.
Compliance with ethical standards
This study was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant (#46205) to John Buckland-Nicks.
Conflict of interest
The authors declare that they have no conflicts of interest.
Studies with human participants
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.
- Bieler R, Mikkelsen PM, Collins TM, Glover ER, Gonzalez VL, Graf DL, Harper EM, Healy J, Kawanski GY, Sharma PP, Staubach S, Strong EE, Taylor JD, Temkin I, Zardus JD, Clark S, Guzman A, McIntyre E, Sharp P, Giribet G (2014) Investigating the Bivalve Tree of Life—an exemplar-based approach combining molecular and novel morphological characters. Invert Syst 28:32–115CrossRefGoogle Scholar
- Boyer BC, Smith GW (1982) Sperm morphology and development in two acoel Turbellarians from the Phillippines. Pacific Sci 36:365–380Google Scholar
- Buckland-Nicks JA (1995) Ultrastructure of sperm and sperm–egg interaction in Aculifera: implications for molluscan phylogeny. In: Jamieson BGM, Ausio J-L, Justine J (eds) Advances in spermatozoal phylogeny and taxonomy, vol 166. Mémoires du Muséum national d’Histoire Naturelle, Paris, pp 129–153Google Scholar
- Buckland-Nicks JA (2006) Fertilization in chitons: morphological clues to phylogeny. Venus 65:51–70Google Scholar
- Buckland-Nicks JA, Chia FS (1986) Formation of the acrosome and basal body during spermiogenesis in a marine snail, Nerita picea (Mollusca: Archaeogastropoda). Mol Reprod Dev 15:13–23Google Scholar
- Franzén Å (1955) Comparative morphological investigations into the spermiogenesis among Mollusca. Zool Bidr Upps 30:399–456Google Scholar
- Haszprunar G (1996) Plathelminthes and Plathelminthomorpha— paraphyletic taxa. J Zool Syst Evol Res 34:41–48. https://doi.org/10.1111/j.1439-0469.1996.tb00808.x CrossRefGoogle Scholar
- Healy JM (1988) Sperm morphology and its systematic importance in the Gastropoda. Malacol Rev Supp 4:251–266Google Scholar
- Healy JM (1996) Molluscan sperm ultrastructure: correlation with taxonomic units within the Gastropoda, Cephalopoda and Bivalvia. In: Taylor J (ed) Origin and evolutionary radiation of the Mollusca. Oxford University Press, Oxford, pp 99–113Google Scholar
- Hejnol A. Obst M, Stamatakis A, Ott M, Rouse GW, Edgecombe GD, Martinez P, Baguna J, Bailly X, Jondelius U, Wiens M, Müller WEG, Seaver E, Wheeler WC, Martindale MQ, Giribet G, Dunn CW (2009) Assessing the root of bilaterian animals with scalable phylogenetic methods. Proc R Soc B 276:4261–4270CrossRefGoogle Scholar
- Hendelberg J (1977) Comparative morphology of turbellarian spermatozoa studied by electron microscopy. Acta Zool 154:149–162Google Scholar
- Justine J-L (2001) Spermatozoa as phylogenetic characters for the Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. CRC Press, Boca Raton, USA, pp 231–238Google Scholar
- Lundin K, Sterrer W (2000) The Nemertodermatida. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. CRC Press, pp 24–27Google Scholar
- Raikova OL, Reuter M, Justine J-L (2001) Contributions to the phylogeny and systematics of the Acoelomorpha. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. CRC Press, Boca Raton, USA, pp 13–23Google Scholar
- Ruiz-Trillo I, Riutort M, Littlewood DT, Herniou EA, Baguña J (1999) Acoel flatworms: earliest extant bilaterian Metazoans, not members of Platyhelminthes. Science 283:1919–1923. https://www.ncbi.nlm.nih.gov/pubmed/10082465
- Ruiz-Trillo I, Paps J, Loukota M, Ribera C, Jondelius U, Baguñá J, Riutort M (2002) A phylogenetic analysis of myosin heavy chain type II sequences corroborates that Acoela and Nemertodermatida are basal bilaterians. Proc Natl Acad Sci 99:11246–11251. https://www.ncbi.nlm.nih.gov/pubmed/12177440
- Tyler S, Rieger RM (1977) Ultrastructural evidence for the systematic position of the Nemertodermatida (Turbellaria). Acta Zool 154:193–207Google Scholar