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Fine structure of spermatids and sperm of Dolioletta gegenbauri and Doliolum nationalis (Tunicata: Thaliacea): implications for tunicate phylogeny

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Abstract

In Dolioletta gegenbauri and Doliolum nationalis, collected in 1987 in the bay of Villefranche-sur-mer (French Mediterranean Sea), spermiogenesis is essentially the same. Early spermatids have a round head, a flagellum arising from a single centriole with short microtubules at 45° to its base, several mitochondria, and an acrosome 50 nm thick and 250 nm long with its long axis parallel to the plasma membrane. The acrosomal contents are dense, with a central denser plate. The nuclear envelope next to the acrosome is thickened and concave. In elongating nuclei, strands of chromatin become oriented parallel to the length of the nucleus and then twist helically. Although the mitochondria surround the nucleus, they remain relatively short and do not fuse into a single mitochondrion as in sperm of other tunicates. In very late doliolid spermatids, the acrosome undergoes exocytosis, and exposes fibrous material that stays associated with the tip of the sperm; no acrosomal tubule forms. Exocytosis at this stage may be triggered by fixation. If so, exocytosis probably occurs naturally at some time before fusion of sperm and egg. Sperm have elongate heads (1 μm×10 μm), with the anterior two-thirds of the nucleus surrounded by mitochondria. Spermiogenesis in doliolids, compared to that in other tunicates, is most like that in solitary members of the class Ascidiacea, except that in the latter the sperm mitochondria fuse and the acrosome appears incapable of exocytosis. In contrast, previous work has shown that salps (class Thaliacea) and colonial didemnid ascidians have an acrosomeless sperm with a spiral mitochondrion, while the class Appendicularia has a sperm with a midpiece, a compact head and an acrosome capable of exocytosis and acrosomal tubule formation. By outgroup comparison with echinoderms and acraniates, appendicularian sperm are plesiomorphic within the Tunicata. Thus, gamete morphology indicates that (1) solitary ascidians and doliolids had a common ancestor, (2) the popular idea that doliolids gave rise to appendicularians is incorrect, and (3) the Thaliacea are polyphyletic, doliolids having arisen very early from the ascidian lineage and salps having arisen later.

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  1. L. Z. Holland

    Present address: A-002, Scripps Institution of Oceanography, University of California at San Diego, 92093, La Jolla, California, USA

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  1. Station Zoologique, B.P. 28, F-06230, Villefranche-sur-mer, France

    L. Z. Holland

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Communicated by P. C. Schroeder, Pullman

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Holland, L.Z. Fine structure of spermatids and sperm of Dolioletta gegenbauri and Doliolum nationalis (Tunicata: Thaliacea): implications for tunicate phylogeny. Mar. Biol. 101, 83–95 (1989). https://doi.org/10.1007/BF00393481

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