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Dicyemid’s dilemma: structure versus genes. The unorthodox structure of dicyemid reproduction

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Abstract

The clear phylogenetic status of the enigmatic Phylum Dicyemida is still uncertain. Their primitive body plan lacks essential metazoan synapomorphies, while genetic data favor a kinship with higher lophotrochozoans. This ultrastructural study increases the confusion about this phylum by presenting an unusual gonad and sperm structure lacking all synapomorphies essential for the various phyla of the lophotrochozoans, either free-living ones or parasites. In Dicyema typus, gonadogenesis is reduced to a single somatic cell, i.e., the infusorigen’s axial cell that functions as a somatic gonadal founder cell as soon as a spermatogonium takes residence in its cytoplasm. The spermiogenic cells resulting therefrom are not connected by intercellular bridges and permanently contain a bundle of microtubules in their cytoplasm, obviously a kind of “dormant” spindle having assembled without centrosomes. Primary spermatocytes develop so-called polycomplexes, multiple synaptinemal complexes. The structure of the sperm is based on a certain kind of somatic cell that has been minimally adapted to function as a sperm. The mature sperm consists in only three organelles: an ovoid nucleus with a somatic chromatin structure, numerous pore complexes and a centrally arranged cluster of coiled tubular structures; a bundle of microtubules embedded into a rim running along the nucleus longitudinal surface, projecting out of the cell like a spear; and a lipid vesicle tightly attached to one pole of the nucleus, touching there the adjacent bundle of microtubules. Immunelectron microscopy confirms the somatic condition of mature sperm, revealing somatic histone H1 immunoreactivity over the nucleus, which can be interpreted as synapomorphy shared with Protozoa, Porifera and Cnidaria. Fertilization occurs as selfing, where the sperm penetrates, “bundle of microtubules first”, a primary oocyte attached vis-à-vis on the other side of the plasma membrane of the infusorigen’s axial cell. This somatic situation points to an ancient evolutionary model rather than to a condition caused by retrogression due to their life as commensals.

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Acknowledgements

The author thanks Ms. Marianne Steiner and Ms. Erika Vanyek for their skilled technical assistance and Ms. Christa Farrenkopf for her competent editorial cooperation.

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  1. Center of Anatomy and Cell Biology, Laboratory of Comparative Cell Biology, Medical University of Vienna, Schwarzspanierstr. 17, 1090, Vienna, Austria

    Renate Czaker

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  1. Renate Czaker
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Correspondence to Renate Czaker.

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Czaker, R. Dicyemid’s dilemma: structure versus genes. The unorthodox structure of dicyemid reproduction. Cell Tissue Res 343, 649–658 (2011). https://doi.org/10.1007/s00441-010-1124-z

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  • DOI: https://doi.org/10.1007/s00441-010-1124-z

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