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Neuroanatomie von Asselspinnen – vergleichende Untersuchungen neuronaler Strukturen zur Klärung von Phylogenie und Evolution einer alten Arthropodenlinie mit begrenzter morphologischer Disparität

Antragsteller Dr. Georg Brenneis
Fachliche Zuordnung Systematik und Morphologie der Tiere
Förderung Förderung von 2018 bis 2022
Projektkennung Deutsche Forschungsgemeinschaft (DFG) - Projektnummer 405578166
 
Erstellungsjahr 2023

Zusammenfassung der Projektergebnisse

As sister group of all other extant chelicerates, the marine Pycnogonida (sea spiders) is an important taxon to study when trying to understand and polarize evolutionary transformations near the base of the chelicerate tree. Prior to the project, neither external morphological characters, nor molecular sequence data had enabled reconstruction of a robust pycnogonid phylogeny, hampering reliable identification of ancestral sea spider traits. For this reason, exploration of internal anatomical characters for phylogenetic inference was a logical next step and the documented usefulness of neural characters in this context rendered exploration of the nervous system highly promising. The project aimed to investigate the adult neuroanatomy of all major pycnogonid taxa ("families”) at various levels of resolution, ranging from gross neuroanatomical features down the cell level. To this end, micro-computed X-ray tomography, immunohistochemical labeling of structural proteins and various neuroactive substances, neuronal backfills and classical histology were synergistically combined and coupled to computer-aided 3D reconstruction for analysis and visualization. Further, embedded in an international collaborative effort, a comprehensive molecular phylogenetic analysis of all eleven pycnogonid families was conducted. The resulting topology represents the first well-supported molecular hypothesis that could be scrutinized for congruence with external morphological and neuroanatomical characters. Unfortunately, the COVID-19 pandemic impeded several of the planned animal collection trips, which for some families led to limited availability of suitably preserved material. In spite of this, several comparative neuroanatomical studies with complete or nearly complete family coverage were performed. (1) The investigation of the pycnogonid brain with a focus on the visual pathway revealed a highly conserved serial layout that features a single visual neuropil connected to a bilayered arcuate body, the latter being for the first time described for sea spiders. This layout shows striking similarities to the median eye pathway of other chelicerates, with additional correspondences to the one of horseshoe crabs, thus indicating it to represent an ancestral chelicerate condition. (2) A µCT-based study provided novel insights at the macro-anatomical level. Several features of the ventral nerve cord with its largely separate segmental ganglia strongly correlate with external morphology, containing thus only limited independent characters for phylogenetic analyses. In four families, however, a ganglionic fusion in the anterior part is observed, which in the case of the families Pycnogonidae and Rhynchothoracidae may support a sister group relationship. (3) 3D reconstructions of the array of intraganglionic tracts and neuropil regions show strong pattern conservation across families. While providing only limited signal for phylogenetic inference within Pycnogonida, these results will allow confident pattern comparison to other euchelicerates in the future. (4) At the cell level, various neuroactive substances are segmentally expressed in stereotypical sets of individually identifiable neurons or small neuron clusters. SIFamidepositive neurons are particularly interesting, as their patterns show intra-familial conservation, but interfamilial differences. Based on parsimony reasoning, the distribution of SIFamide patterns aligns well with the latest molecular phylogeny and stands in contrast to external morphology-based groupings. Beyond neuroanatomy, part of the material collected was used for an integrative taxonomic study that resulted in the reinstatement of the genus Pallenella and the description of two species new to science. Additionally, regeneration studies revealed exceptional resilience of pycnogonids to traumatic injury and provided the first report of complex primary body axis regeneration in an arthropod. Given the phylogenetic position of sea spiders, this could potentially represent a plesiomorphic arthropod trait.

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