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Olfactory pathway in Xibalbanus tulumensis: remipedian hemiellipsoid body as homologue of hexapod mushroom body

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Abstract

The Remipedia have been proposed to be the crustacean sister group of the Hexapoda. These blind cave animals heavily rely on their chemical sense and are thus rewarding subjects for the analysis of olfactory pathways. The evolution of these pathways as a character for arthropod phylogeny has recently received increasing attention. Here, we investigate the situation in Xibalbanus tulumensis by focal dye injections and immunolabelling of the catalytic subunit of the cAMP-dependent protein kinase (DC0), an enzyme particularly enriched in insect mushroom bodies. DC0 labelling of the hemiellipsoid body suggests its subdivision into a cap-like and a core neuropil. Immunofluorescence of the enzyme glutamic acid decarboxylase (GAD), which synthesizes γ-aminobutyric acid (GABA), has revealed a cluster of GABAergic interneurons in the hemiellipsoid body, reminiscent of the characteristic feedback neurons of the mushroom body. Thus, the hemiellipsoid body of Xibalbanus shares many of the characteristics of insect mushroom bodies. Nevertheless, the general neuroanatomy of the olfactory pathway in the Remipedia strongly corresponds to the malacostracan ground pattern. Given that the Remipedia are probably the sister group of the Hexapoda, the phylogenetic appearance of the typical neuropilar compartments in the insect mushroom body has to be assigned to the origins of the Hexapoda.

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Acknowledgments

We thank Dr. Daniel Kalderon for the gift of the DC0 antibody. We are grateful to Hannah Scheiblich for sharing her expertise in western blot analysis with us. René Eickhoff and Michael Stern contributed stimulating discussions and helpful comments. A collecting permit for Remipedia was issued by SEMARNAT (Secretaría de Medio Ambiente y Recursos Naturales) to Thomas M. Iliffe via a permit to Dr. Fernando Alvarez (FAUT-0104). The landowner kindly gave permission to collect specimens on the site.

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Authors and Affiliations

  1. Division of Cell Biology, University of Veterinary Medicine Hannover, Bischhofsholer Damm 15, 30173, Hannover, Germany

    Torben Stemme & Gerd Bicker

  2. Department of Marine Biology, Texas A&M University at Galveston, 200 Seawolf Parkway, Galveston, TX, 77553, USA

    Thomas M. Iliffe

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  1. Torben Stemme
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  2. Thomas M. Iliffe
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Correspondence to Gerd Bicker.

Additional information

This research was supported by a scholarship from the German National Academic Foundation (Studienstiftung des Deutschen Volkes) to Torben Stemme and partly by DFG grant BI 262/18-1. Funds for the collection of Remipedia were provided by Texas A&M University: CONACYT collaborative science grant no. 10655 to Thomas Iliffe and Fernando Alvarez (Universidad Nacional Autónoma de México, Mexico City) and CONACYT grant no. 155644 to Fernando Alvarez.

The authors declare no competing interests.

T.S. carried out the laboratory work, microscopy, interpretation and presentation of data and drafted the manuscript. T.M.I. collected and preserved specimens and helped draft the manuscript. G.B. designed and coordinated the study and helped draft the manuscript. All authors gave final approval for publication.

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Stemme, T., Iliffe, T.M. & Bicker, G. Olfactory pathway in Xibalbanus tulumensis: remipedian hemiellipsoid body as homologue of hexapod mushroom body. Cell Tissue Res 363, 635–648 (2016). https://doi.org/10.1007/s00441-015-2275-8

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