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Early development of the olfactory organ in sturgeons of the genus Acipenser: a comparative and electron microscopic study

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Abstract

Formation and morphology of the olfactory organ of vertebrates has been intensely studied in some taxa for more than a century. As a functionally important and complex sensory organ, its ontogenetic development has often been a matter of debate on higher-level craniate evolution. However, sufficient knowledge of structure and development of the olfactory organ in the crucial taxa needed for a serious phylogenetic reasoning is generally not available. This study aims at this essential primary data source, the detailed structure, morphogenesis, and character definition of the olfactory organ in more basal clades of jawed vertebrates (Gnathostomata). Sturgeon fishes (Acipenseriformes) as recent basal actinopterygians are expected to provide insight into archaic characters and character combinations in bony fishes. Thus, the development of the olfactory placodes of the sterlet, Acipenser ruthenus, and the Siberian sturgeon, Acipenser baerii, was followed histologically, by semi-thin serial sections, and by scanning and transmission electron microscopy. Except for the timing, virtually no differences were observed between the two species. The olfactory placodes become two-layered early in embryonic development. Both the superficial epidermal and the subepidermal layer can easily be distinguished and their development followed by ultrastructural properties. There are three different types of receptor cells: ciliated, microvillous, and crypt cells. The development of the ciliated and the less abundant microvillous receptor cells from the subepidermal layer of the placode is demonstrated. The non-sensory cells of the differentiated olfactory epithelium, i.e. ciliated non-sensory cells and supporting cells, exclusively derive from the superficial epidermal layer. In this respect, acipenserids clearly demonstrate close resemblance to the morphogenetic process found in the tetrapod Xenopus (Anura). The only other adequately described mode found in the actinopterygian zebrafish (Danio rerio), is considered a derived character. In this case, all cells of the differentiated olfactory epithelium derive from one placodal cell layer. The mode of formation of the nasal sac and its ventilatory openings found in the acipenserids examined here, represents a widespread and probably a plesiomorphic condition of osteognathostomes. In both species, differentiation of the basic cellular composition of the olfactory epithelium is far advanced at the time of onset of extrinsic feeding.

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Abbreviations

AF :

After fertilization

AH :

After hatching

LM :

Light microscopy

SEM :

Scanning electron microscopy

TEM :

Transmission electron microscopy

ORN :

Olfactory receptor neuron

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Acknowledgements

The authors thank Dr. Bernd Schmeller and his staff (Störnstein, Germany) for providing sterlet eggs and ample help in raising the embryos and larvae. Thanks are also due to Brigitte Segner, Karin Meyer, Martina Wichmann, Renate Walter for their skillful assistance with TEM and SEM preparations.

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Authors and Affiliations

  1. Zoologisches Institut und Zoologisches Museum, Universität Hamburg, Martin-Luther-King-Platz 3, 20146 , Hamburg, Germany

    Eckart Zeiske

  2. Department of Ichthyology, State University of Moscow, Moscow 119899, Russia

    Alexander Kasumyan

  3. Museum für Naturkunde der Humboldt-Universität zu Berlin, Berlin, Germany

    Peter Bartsch

  4. Cellular and Structural Biology, University of Colorado Health Sciences Center, 4200 East 9th Ave., Campus Box B111, Denver, CO 80262, USA

    Anne Hansen

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  1. Eckart Zeiske
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  2. Alexander Kasumyan
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  4. Anne Hansen
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Correspondence to Anne Hansen.

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Zeiske, E., Kasumyan, A., Bartsch, P. et al. Early development of the olfactory organ in sturgeons of the genus Acipenser: a comparative and electron microscopic study. Anat Embryol 206, 357–372 (2003). https://doi.org/10.1007/s00429-003-0309-6

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