A microCT-based atlas of the central nervous system and midgut in sea spiders (Pycnogonida) sheds first light on evolutionary trends at the family level

• Published in: Frontiers in zoology Vol. 19; no. 1; p. 14
• Main Authors: Frankowski, Karina, Miyazaki, Katsumi, Brenneis, Georg
• Format: Journal Article
• Language: English
• Published: England BioMed Central Ltd 31-03-2022; BioMed Central; BMC
• Subjects: Anatomy; Arthropods; Central nervous system; Chelicerata; Computed tomography; CT imaging; Digestive system; Evolution; Ganglia; Genetic aspects; Midgut; Morphology; Muscles; Nervous system; Neuroanatomy; Pantopoda; Phylogenetics; Phylogeny; Physiological aspects; Pycnogonida; Pycnogonidae; Sea spiders; Synapsin; Tubulin; Ventral nerve cord; Japan; Pantopoda; 3D reconstruction; Digestive system; Neuroanatomy; X-ray tomography; Chelicerata; Evolution; Phylogeny; Ventral nerve cord
• ISSN: 1742-9994; 1742-9994
• DOI: 10.1186/s12983-022-00459-8

Pycnogonida (sea spiders) is the sister group of all other extant chelicerates (spiders, scorpions and relatives) and thus represents an important taxon to inform early chelicerate evolution. Notably, phylogenetic analyses have challenged traditional hypotheses on the relationships of the major pycnogonid lineages (families), indicating external morphological traits previously used to deduce inter-familial affinities to be highly homoplastic. This erodes some of the support for phylogenetic information content in external morphology and calls for the study of additional data classes to test and underpin in-group relationships advocated in molecular analyses. In this regard, pycnogonid internal anatomy remains largely unexplored and taxon coverage in the studies available is limited.
Based on micro-computed X-ray tomography and 3D reconstruction, we created a comprehensive atlas of in-situ representations of the central nervous system and midgut layout in all pycnogonid families. Beyond that, immunolabeling for tubulin and synapsin was used to reveal selected details of ganglionic architecture. The ventral nerve cord consistently features an array of separate ganglia, but some lineages exhibit extended composite ganglia, due to neuromere fusion. Further, inter-ganglionic distances and ganglion positions relative to segment borders vary, with an anterior shift in several families. Intersegmental nerves target longitudinal muscles and are lacking if the latter are reduced. Across families, the midgut displays linear leg diverticula. In Pycnogonidae, however, complex multi-branching diverticula occur, which may be evolutionarily correlated with a reduction of the heart.
Several gross neuroanatomical features are linked to external morphology, including intersegmental nerve reduction in concert with trunk segment fusion, or antero-posterior ganglion shifts in partial correlation to trunk elongation/compaction. Mapping on a recent phylogenomic phylogeny shows disjunct distributions of these traits. Other characters show no such dependency and help to underpin closer affinities in sub-branches of the pycnogonid tree, as exemplified by the tripartite subesophageal ganglion of Pycnogonidae and Rhynchothoracidae. Building on this gross anatomical atlas, future studies should now aim to leverage the full potential of neuroanatomy for phylogenetic interrogation by deciphering pycnogonid nervous system architecture in more detail, given that pioneering work on neuron subsets revealed complex character sets with unequivocal homologies across some families.