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Comparative ultrastructure of the spermatogenesis of three species of Poecilosclerida (Porifera, Demospongiae)

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Abstract

The spermatogenesis of Porifera is still relatively poorly understood. In the past, it was accepted that all species presented a primitive-type spermatozoon, lacking special structures and acrosome. Nonetheless, a very peculiar spermatogenesis resulting in a sophisticated V-shaped spermatozoon with an acrosome was found in Poecilosclerida. This finding called into question the diversity and evolution of sperm cells in Poecilosclerida and in Porifera, as a whole. Is this sophisticated spermatozoon widespread in the group? We investigated here the ultrastructure of the spermatogenesis of three different species of Poecilosclerida (Demospongiae): Iophon proximum, I. piceum, and Tedania ignis. In all three species, spermatogenesis was synchronized within the spermatic cysts. Iophon proximum and T. ignis presented elongated sperm cells, but in I. piceum, their shape was oblong. A structure resembling an acrosome was only found in T. ignis. All three species presented modified spermatozoa, as in the majority of poecilosclerids investigated so far. Therefore, we are proposing that the elongated shape (modified type) of spermatozoon is the ancestral state based in the current phylogeny of Poecilosclerida and that the V-shaped sperm is only found in Crambeidae.

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Abbreviations

MNRJ:

Museu Nacional do Rio de Janeiro, Brazil

RBINS:

Royal Belgian Institute of Natural Sciences

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Acknowledgements

We would like to thank the staff at the Serviços de Microscopia Eletrônica-CPqGM-Fiocruz for help with the preparation of the samples of T. ignis. The present work is part of the PhD thesis of VV presented at the PPG em Diversidade Animal of the Federal University of Bahia. PhW and AE are indebted to Profs I. Eeckhaut and P. Flammang, Laboratoire de Biologie Marine, Université de Mons for their cordial reception in the TEM facilities under their care. Profs E. Pays and D. Pérez-Morga are also thanked for welcoming us in the Centre for Microscopy and Molecular Imaging of the Université Libre de Bruxelles. J. Cillis (RBINS) gave us technical support of with the SEM. We are grateful to G. Försterra and V. Häussermann (Huinay Scientific Field Station, Chile) and the Huinay Foundation without whom collecting Iophon proximum would not have been possible. Both are further thanked, as well as R. Fitzek and S. González for the hospitality and exceptional logistic support received at the Huinay Scientific Field Station. AE is grateful to the Marine Biological Station (ERS “Belomorskaia”) of St. Petersburg State University for technical support.

Funding

EL and VV thank the Foundation for Researcher Support of the State of Bahia (FAPESB—Grant no. JCB0014/2016) and the National Council for Scientific and Technological Development (CNPq—Grant no. 477227/2013-9) for the financial assistance. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. The Belgian Federal Science Policy Office funded the work of AE at the RBINS (S&T Grant for collaboration with Oriental and Central Europe) as well as fieldwork of PhW in Chile (CALMARS I-contract EV/03/04B). This is publication Number 162 from the Huinay Scientific Field Station.

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Correspondence to Emilio Lanna.

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The authors declare that they have no conflict of interest. This article does not contain any studies with human participants performed by any of the authors. Brazilian sample collections were carried out under the license of ICMBIO (#9321-1). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

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Vasconcellos, V., Willenz, P., Ereskovsky, A. et al. Comparative ultrastructure of the spermatogenesis of three species of Poecilosclerida (Porifera, Demospongiae). Zoomorphology 138, 1–12 (2019). https://doi.org/10.1007/s00435-018-0429-4

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  • DOI: https://doi.org/10.1007/s00435-018-0429-4

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