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Front. Ecol. Evol. | doi: 10.3389/fevo.2017.00151

Multiple identified neurons and peripheral nerves innervating the prothoracic defense glands in stick insects reveal evolutionary conserved and novel elements of a chemical defense system

 Johannes Strauß1*,  Christoph-Rüdiger von Bredow2,  Yvette M. von Bredow2, Konrad Stolz1, Tina E. Trenczek2 and Reinhard Lakes-Harlan1*
  • 1Institute for Animal Physiology, Justus Liebig Universität Gießen, Germany
  • 2Institute for General and Applied Zoology, Justus Liebig Universität Gießen, Germany

The defense glands in the dorsal prothorax are an important autapomorphic trait of stick insects (Phasmatodea). Here, we study the functional anatomy and neuronal innervation of the defense glands in Anisomorpha paromalus (Westwood, 1859) (Pseudophasmatinae), a species which sprays its defense secretions when disturbed or attacked. We use a neuroanatomical approach to identify the nerves innervating the gland muscles and the motoneurons with axons in the different nerves. The defense gland is innervated by nerves originating from two segments, the suboesophageal ganglion and the prothoracic ganglion. Axonal tracing confirms the gland innervation via the anterior suboesophageal nerve, and two intersegmental nerves, the posterior suboesophageal nerve and the anterior prothoracic nerve. Axonal tracing of individual nerves reveals eight identified neuron types in the suboesophageal or prothoracic ganglion. The strongest innervating nerve of the gland is the anterior suboesophageal nerve, which also supplies dorsal longitudinal thorax muscles (neck muscles) by separate nerve branches. Tracing of individual nerve branches reveals different sets of motoneurons innervating the defense gland (one ipsilateral and one contralateral suboesophageal neuron) or the neck muscle (ventral median neurons). The ipsilateral and contralateral suboesophageal neurons have no homologs in related taxa like locusts and crickets, and thus evolved within stick insects with the differentiation of the defense glands. The overall innervation pattern suggests that the longitudinal gland muscles derived from dorsal longitudinal neck muscles. In sum, the innervating nerves for dorsal longitudinal muscles are conserved in stick insects, while the neuronal control system was specialized with conserved motoneurons for the persisting neck muscles, and evolutionarily novel suboesophageal and prothoracic motoneurons innervating the defense gland.

Keywords: stick insect, Neuroanatomy, defense gland, innervation, motoneurons

Received: 30 Sep 2017; Accepted: 14 Nov 2017.

Edited by:

Sven Bradler, University of Göttingen, Germany

Reviewed by:

Fanny Leubner, University of Göttingen, Germany
Thomas Van De Kamp, Karlsruhe Institute of Technology, Germany  

Copyright: © 2017 Strauß, von Bredow, von Bredow, Stolz, Trenczek and Lakes-Harlan. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence:
Dr. Johannes Strauß, Justus Liebig Universität Gießen, Institute for Animal Physiology, IFZ - Heinrich-Buff-Ring 26, Giessen, 35392, Germany,
Prof. Reinhard Lakes-Harlan, Justus Liebig Universität Gießen, Institute for Animal Physiology, IFZ - Heinrich-Buff-Ring 26, Giessen, 35392, Germany,