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Unexpected ultrastructure of an eye in Spiralia: the larval ocelli of Procephalothrix oestrymnicus (Nemertea)

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Abstract

The evolution of eyes and their constituent photoreceptor cells in Metazoa in general and in Protostomia in particular remains unresolved with present morphological and developmental genetic data. This is mainly due to the lack of comprehensive ultrastructural data in some lineages, such as in the spiralian taxon Nemertea. The eyes of the derived Neonemertea possess rhabdomeric photoreceptor cells, considered typical of the protostome lineage. In the more basally branching palaeonemertean lineages, ultrastructural data on the eyes are wanting. Ultrastructural investigation of the eyes of the larva of the palaeonemertean Procephalothrix oestrymnicus reveals that, although in a similar position as the eyes of adult neonemertean species, the eyes in palaeonemertean larvae differ fundamentally from the expected protostomian type: They consist of one shading-pigment cell that forms a closed optical cavity embedded in the epidermis. Apart from basally distributed shading-pigment vesicles, the pigment cell apically possesses epidermal cilia and microvilli as well as sub-apical, tubular lens vesicles. Two ciliary photoreceptor cells project flattened ciliary membranes into the optical cavity formed by the pigment cell, whereas their basal portions are situated outside of the optical cavity, next to the shading-pigment cell. Although the structure of the eye in P. oestrymnicus is unparalleled in Nemertea, ciliary photoreceptor cells have been found in larval eyes of several other spiralian lineages. Occurrence of additional ciliary-type eyes in Spiralia deepens the doubts regarding the validity of the hypothesis of an exclusively rhabdomeric line of visual photoreceptor cell evolution in Protostomia.

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Acknowledgements

The staff of the Station de Biologie Marine et Marinarium de Concarneau is gratefully acknowledged for providing facilities while collecting and rearing of Procephalothrix oestrymnicus.

Funding

The investigation was financially supported by the German Research Council (DFG, Ba 1520/11-1,2).

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  1. Institute of Evolutionary Biology and Ecology, University of Bonn, Bonn, Germany

    Jörn von Döhren & Thomas Bartolomaeus

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  1. Jörn von Döhren
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Correspondence to Jörn von Döhren.

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All applicable international, national and/or institutional guidelines for the care and use of animals were followed. We neither used endangered species nor were the investigated animals collected in protected areas. All animals were collected with the permission of the local marine biological station, the Station de Biologie Marine, Concarneau (France).

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von Döhren, J., Bartolomaeus, T. Unexpected ultrastructure of an eye in Spiralia: the larval ocelli of Procephalothrix oestrymnicus (Nemertea). Zoomorphology 137, 241–248 (2018). https://doi.org/10.1007/s00435-017-0394-3

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