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The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives

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Abstract

Understanding the origin and evolution of arthropods requires examining their closest outgroups, the tardigrades (water bears) and onychophorans (velvet worms). Despite the rise of molecular techniques, the phylogenetic positions of tardigrades and onychophorans in the panarthropod tree (onychophorans + tardigrades + arthropods) remain unresolved. Hence, these methods alone are currently insufficient for clarifying the panarthropod topology. Therefore, the evolution of different morphological traits, such as one of the most intriguing features of panarthropods—their nervous system—becomes essential for shedding light on the origin and evolution of arthropods and their relatives within the Panarthropoda. In this review, we summarise current knowledge of the evolution of panarthropod nervous and visual systems. In particular, we focus on the evolution of segmental ganglia, the segmental identity of brain regions, and the visual system from morphological and developmental perspectives. In so doing, we address some of the many controversies surrounding these topics, such as the homology of the onychophoran eyes to those of arthropods as well as the segmentation of the tardigrade brain. Finally, we attempt to reconstruct the most likely state of these systems in the last common ancestors of arthropods and panarthropods based on what is currently known about tardigrades and onychophorans.

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Acknowledgements

We are thankful to Noel N. Tait for his assistance with the permits and to Dave M. Rowell, Paul Sunnucks, Noel N. Tait, Franziska A. Franke, Sandra Treffkorn and Michael Gerth for helping to collect the specimens. We also thank Nicole Naumann for assistance with immunohistochemistry, Jörg U. Hammel for his help with SRµCT and all members of the Mayer laboratory for helping with animal husbandry. We gratefully acknowledge Bert R. E. Klagges for providing the anti-synapsin serum. Two anonymous reviewers provided constructive comments, which helped to improve the manuscript. This study was supported by a German Academic Exchange Service (DAAD) scholarship to VG; a Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq Brazil: 290029/2010-4) Grant to ISO; a Helmholtz Research Centre Grant (DESY: I-20150213) and the Emmy Noether Programme Funding (Ma 4147/3-1), and an additional Grant (Ma 4147/8-1) of the German Research Foundation (DFG) to GM.

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Authors and Affiliations

  1. Department of Zoology, University of Kassel, Heinrich-Plett-Str. 40, 34132, Kassel, Germany

    Christine Martin, Vladimir Gross, Lars Hering, Benjamin Tepper, Henry Jahn, Ivo de Sena Oliveira & Georg Mayer

  2. Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos 6627, Belo Horizonte, 31270-901, Brazil

    Ivo de Sena Oliveira

  3. Physiology of Animals and Behaviour, Institute of Biology, University of Leipzig, Talstraße 33, 04103, Leipzig, Germany

    Paul Anthony Stevenson

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  1. Christine Martin
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  2. Vladimir Gross
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Correspondence to Georg Mayer.

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Martin, C., Gross, V., Hering, L. et al. The nervous and visual systems of onychophorans and tardigrades: learning about arthropod evolution from their closest relatives. J Comp Physiol A 203, 565–590 (2017). https://doi.org/10.1007/s00359-017-1186-4

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  • DOI: https://doi.org/10.1007/s00359-017-1186-4

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