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.