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Sex in the beach: spermatophores, dermal insemination and 3D sperm ultrastructure of the aphallic mesopsammic Pontohedyle milaschewitchii (Acochlidia, Opisthobranchia, Gastropoda)

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Abstract

Sperm transfer via spermatophores is common among organisms living in mesopsammic environments, and is generally considered to be an evolutionary adaptation to reproductive constraints in this habitat. However, conclusions about adaptations and trends in insemination across all interstitial taxa cannot be certain as differences in mode of insemination via spermatophores do exist, details of insemination are lacking for many species, and evolutionary relationships in many cases are poorly known. Opisthobranch gastropods typically transfer sperm via reciprocal copulation, but many mesopsammic Acochlidia are aphallic and transfer sperm via spermatophores, supposedly combined with dermal fertilisation. The present study investigates structural and functional aspects of sperm transfer in the Mediterranean microhedylacean acochlid Pontohedyle milaschewitchii. We show that spermatophore attachment is imprecise. We describe the histology and ultrastructure of the two-layered spermatophore and discuss possible functions. Using DAPI staining of the (sperm-) nuclei, we document true dermal insemination in situ under the fluorescence microscope. Ultrastructural investigation and computer-based 3D reconstruction from TEM sections visualise the entire spermatozoon including the exceptionally elongate, screw-like keeled sperm nucleus. An acrosomal complex was not detected. From their special structure and behaviour we conclude that sperm penetrate epithelia, tissues and cells mechanically by drilling rather than lysis. Among opisthobranchs, dermal insemination is limited to mesopsammic acochlidian species. In this spatially limited environment, a rapid though imprecise and potentially harmful dermal insemination is discussed as a key evolutionary innovation that could have enabled the species diversification of microhedylacean acochlidians.

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Acknowledgments

We wish to thank Eva Lodde (ZSM) and Heidi Gensler (Department Biology I, LMU) for expert help in histological techniques. Roland Melzer (ZSM) is thanked for supporting DAPI staining and Roland Meyer (ZSM) for his company and help in collecting specimens. We also thank Thomas Heinzeller and Birgit Aschauer (Anatomische Anstalt, LMU) for the provision of the TEM. The study was partially financed by a grant of the German Research Foundation to MS (DFG SCHR 667-4). Computer-based 3D-reconstruction using AMIRA® software was supported by the GeoBioCenter LMU/Germany. Three anonymous reviewers are acknowledged for helpful comments on the manuscript.

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Authors and Affiliations

  1. Zoologische Staatssammlung München, Münchhausenstraße 21, 81247, Munich, Germany

    Katharina Maria Jörger, Timea Pamela Neusser & Michael Schrödl

  2. Department Biology I, Ludwig-Maximilians-Universität München, Großhadener Str. 2-4, 85152, Planegg-Martinsried, Germany

    Martin Heß

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  1. Katharina Maria Jörger
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  2. Martin Heß
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  3. Timea Pamela Neusser
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Correspondence to Katharina Maria Jörger.

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Communicated by M. Byrne.

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Jörger, K.M., Heß, M., Neusser, T.P. et al. Sex in the beach: spermatophores, dermal insemination and 3D sperm ultrastructure of the aphallic mesopsammic Pontohedyle milaschewitchii (Acochlidia, Opisthobranchia, Gastropoda). Mar Biol 156, 1159–1170 (2009). https://doi.org/10.1007/s00227-009-1158-5

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