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Open Access Highly Accessed Research article

Selective neuronal staining in tardigrades and onychophorans provides insights into the evolution of segmental ganglia in panarthropods

Georg Mayer1*, Christine Martin1, Jan Rüdiger1, Susann Kauschke1, Paul A Stevenson2, Izabela Poprawa3, Karin Hohberg4, Ralph O Schill5, Hans-Joachim Pflüger6 and Martin Schlegel78

Author affiliations

1 Animal Evolution and Development, Institute of Biology, University of Leipzig, Talstraße 33, D-04103 Leipzig, Germany

2 Physiology of Animals and Behavior, Institute of Biology, University of Leipzig, Talstraße 33,D-04103 Leipzig, Germany

3 Department of Animal Histology and Embryology, University of Silesia, Bankowa 9, 40-007 Katowice, Poland

4 Senckenberg Museum of Natural History Görlitz, Am Museum 1, D-02826 Görlitz, Germany

5 Biological Institute, Zoology, University of Stuttgart, Pfaffenwaldring 57, D-70569 Stuttgart, Germany

6 Neurobiology, Institute of Biology, Freie Universität Berlin, Königin-Luise-Str. 28-30, D-14195 Berlin, Germany

7 Molecular Evolution & Animal Systematics, Institute of Biology, University of Leipzig, Talstraße 33, D-04103 Leipzig, Germany

8 German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-Leipzig, Deutscher Platz 5e, D-04103 Leipzig, Germany

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Citation and License

BMC Evolutionary Biology 2013, 13:230  doi:10.1186/1471-2148-13-230

Published: 24 October 2013

Abstract

Background

Although molecular analyses have contributed to a better resolution of the animal tree of life, the phylogenetic position of tardigrades (water bears) is still controversial, as they have been united alternatively with nematodes, arthropods, onychophorans (velvet worms), or onychophorans plus arthropods. Depending on the hypothesis favoured, segmental ganglia in tardigrades and arthropods might either have evolved independently, or they might well be homologous, suggesting that they were either lost in onychophorans or are a synapomorphy of tardigrades and arthropods. To evaluate these alternatives, we analysed the organisation of the nervous system in three tardigrade species using antisera directed against tyrosinated and acetylated tubulin, the amine transmitter serotonin, and the invertebrate neuropeptides FMRFamide, allatostatin and perisulfakinin. In addition, we performed retrograde staining of nerves in the onychophoran Euperipatoides rowelli in order to compare the serial locations of motor neurons within the nervous system relative to the appendages they serve in arthropods, tardigrades and onychophorans.

Results

Contrary to a previous report from a Macrobiotus species, our immunocytochemical and electron microscopic data revealed contralateral fibres and bundles of neurites in each trunk ganglion of three tardigrade species, including Macrobiotus cf. harmsworthi, Paramacrobiotus richtersi and Hypsibius dujardini. Moreover, we identified additional, extra-ganglionic commissures in the interpedal regions bridging the paired longitudinal connectives. Within the ganglia we found serially repeated sets of serotonin- and RFamid-like immunoreactive neurons. Furthermore, our data show that the trunk ganglia of tardigrades, which include the somata of motor neurons, are shifted anteriorly with respect to each corresponding leg pair, whereas no such shift is evident in the arrangement of motor neurons in the onychophoran nerve cords.

Conclusions

Taken together, these data reveal three major correspondences between the segmental ganglia of tardigrades and arthropods, including (i) contralateral projections and commissures in each ganglion, (ii) segmentally repeated sets of immunoreactive neurons, and (iii) an anteriorly shifted (parasegmental) position of ganglia. These correspondences support the homology of segmental ganglia in tardigrades and arthropods, suggesting that these structures were either lost in Onychophora or, alternatively, evolved in the tardigrade/arthropod lineage.

Keywords:
Arthropoda; Ecdysozoa; Nervous system; Onychophora; Panarthropoda; Segmental ganglia; Synapomorphy; Tardigrada