Similar but different: Comparative neuroanatomy of the chemo- and mechanosensory pathways in scorpion pectines

• Applicant: Dr. Torben Stemme
• Subject Area: Systematics and Morphology (Zoology) ; Evolutionary Cell and Developmental Biology (Zoology)
• Term: from 2018 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 418446511

• Final Report Year: 2023

Final Report Abstract

Sensory abilities are of pivotal importance for almost all animals to navigate their environment and secure survival and reproduction. While insects, crustaceans, and myriapods possess dedicated chemosensory appendages associated with the second head neuromere, the remaining arthropod taxon, the chelicerates, evolved distinct sensory organs in rather different positions. A fascinating example are scorpions, which possess so-called pectines on their ventral body side, directly behind the last walking leg pair. These organs function as bimodal sensors for chemo- and mechanosensory cues on the substrate. Pectines thus fulfil similar functions as antennae, but occupy a different position on the body. Detailed investigation of the associated neuronal pathway is crucial for the understanding of sensory processing, not least in comparison to the antennal pathway of the other arthropod groups. We employed modern neuroanatomical methods, including combinations of immunolabeling, anterograde and lipophilic tracing, confocal laser-scanning microscopy and computer aided-3D- reconstructions, to describe the general anatomy of the pecten neuropils, their innervation by bimodal chemo- and mechanosensory pecten teeth sensilla, and by unimodal mechanosensory hairs. We further analysed the neuroanatomy of the scorpion mushroom body, the most likely upstream integration centre of signals from the pecten neuropils. In order to reveal species-specific differences in pecten pathway stations and higher integration centres, we investigated several scorpion species, occupying different habitats and positions in the scorpion phylogenetic tree. In addition to general similarities, we observed species-specific features in pecten and mushroom body neuroanatomies. This raises the idea that the neuroanatomy of the pecten pathway reflects not only phylogenetic relationships but also a species’ habitat and its degree of sociality. We further demonstrate that afferents from unimodal mechanosensory (hair sensilla) neurons project to a distinct neuropil structure in the nervous system, suggesting a role in reflexive adjustment of body height, obstacle avoidance and mediating of accurate pecten teeth alignment to maintain pectines functionality. Concerning afferents of the bimodal pecten teeth sensilla, we found good evidence that both, chemoand mechanosensory afferents innervate the pecten neuropil in a somatotopic fashion. Although this needs further scrutiny, this finding is highly interesting as such an arrangement is unique to our knowledge.

Publications

• Chemosensory pathways in scorpions and sun spiders. Gordon Research Conference 2019 on Behavior, Evolution and Neurobiology (Multimodal Strategies for Behavioral Control: Molecules, Neurons, Circuits and Behavior), Mount Snow, Vermont (USA) 28/07-02/08/2019.
  Wolf H., Drozd D. & Stemme T.
  
• Histaminergic interneurons in the ventral nerve cord: assessment of their value for Euarthropod phylogeny. Zoological Letters, 5(1).
  Maurer, Maite; Hladik, Janina; Iliffe, Thomas M. & Stemme, Torben
  
• Map-like representation of chemosensory input in the synganglion of two scorpion species. 30th NeuroDoWo, University of Würzburg (Germany) 28-31/08/2019.
  Drozd D., Wolf H. & Stemme T.
  
• Size Matters - Territoriality and Shelter Selection in a Scorpion. 112th Annual Meeting of the German Zoological Society, Jena (Germany) 10-13/09/2019.
  Hladik J. & Stemme T.
  
• Non-visual homing and the current status of navigation in scorpions. Animal Cognition, 23(6), 1215-1234.
  Prévost, Emily Danielle & Stemme, Torben
  
• Structure of the pecten neuropil pathway and its innervation by bimodal peg afferents in two scorpion species. PLOS ONE, 15(12), e0243753.
  Drozd, Denise; Wolf, Harald & Stemme, Torben
  
• Anatomy of the Nervous System in Chelifer cancroides (Arachnida: Pseudoscorpiones) with a Distinct Sensory Pathway Associated with the Pedipalps. Insects, 13(1), 25.
  Stemme, Torben & Pfeffer, Sarah E.
  
• Comparison of chemosensory pathways in Arachnida – insights from a neuroanatomical and behavioral approach. 113th Annual Meeting of the German Zoological Society, virtual format, 30/08-03/09/2021.
  Stemme T.
  
• Home sweet home: Effect of size and scent on shelter selection in two scorpion species. 113th Annual Meeting of the German Zoological Society, virtual format, 30/08-03/09/2021.
  Hladik J. & Stemme T.
  
• Innervation areas of mechanosensory hair sensillae on the scorpion pectines. 113th Annual Meeting of the German Zoological Society, virtual format, 30/08-03/09/2021.
  Drozd D., Wolf H. & Stemme T.
  
• Feels like home: influence of size and chemosensory cues on scorpion shelter choice. International Congress of Neuroethology, Lisbon (Portugal) 24- 29/07/2022.
  Hladik J. & Stemme T.
  
• Mechanosensory pathways of scorpion pecten hair sensillae—Adjustment of body height and pecten position. Journal of Comparative Neurology, 530(16), 2918-2937.
  Drozd, Denise; Wolf, Harald & Stemme, Torben
  
• Unravelling the sensory capabilities of scorpion pectines with a neuroanatomical and behavioural approach. International Congress of Neuroethology, Lisbon (Portugal) 24-29/07/2022.
  Stemme T. & Wolf H.
  
• No evidence for regeneration of pectines in the scorpion Euscorpius italicus (Herbst, 1800). Acta Zoologica, 105(3), 281-293.
  Stemme, Torben