Atlas of the neuromuscular system in the Trachymedusa Aglantha digitale: Insights from the advanced hydrozoan. Issue 7 (2nd December 2019)

• Record Type: Journal Article
• Authors: Norekian, Tigran P.; Moroz, Leonid L.
• Is Part Of: Journal of comparative neurology. Volume 528:Issue 7(2020)
• Page Start: 1231
• Page End: 1254
• Publication Date: 2019-12-02
• Subjects: cell atlas -- Cnidaria -- evolution -- hydra -- muscle system -- nematocysts -- Nematostella -- nervous system -- sensory cells; Comparative neurobiology -- Periodicals; Neurology -- Periodicals; 616
• DOI: 10.1002/cne.24821
• Languages: English
• ISSNs: 0021-9967

Abstract

Abstract: Cnidaria is the sister taxon to bilaterian animals, and therefore, represents a key reference lineage to understand early origins and evolution of the neural systems. The hydromedusa Aglantha digitale is arguably the best electrophysiologically studied jellyfish because of its system of giant axons and unique fast swimming/escape behaviors. Here, using a combination of scanning electron microscopy and immunohistochemistry together with phalloidin labeling, we systematically characterize both neural and muscular systems in Aglantha, summarizing and expanding further the previous knowledge on the microscopic neuroanatomy of this crucial reference species. We found that the majority, if not all (~2, 500) neurons, that are labeled by FMRFamide antibody are different from those revealed by anti‐α‐tubulin immunostaining, making these two neuronal markers complementary to each other and, therefore, expanding the diversity of neural elements in Aglantha with two distinct neural subsystems. Our data uncovered the complex organization of neural networks forming a functional "annulus‐type" central nervous system with three subsets of giant axons, dozen subtypes of neurons, muscles, and a variety of receptors fully integrated with epithelial conductive pathways supporting swimming, escape and feeding behaviors. The observed unique adaptations within the Aglantha lineage (including giant axons innervating striated muscles) strongly support an extensive and wide‐spread parallel evolution of integrative and effector systems across Metazoa. Abstract : We provide a comprehensive atlas of the neuro‐muscular organization in the hydrozoan medusa Aglantha digitale (Cnidaria), revealing unique systems of giant axons, dozens of distinct neuronal, receptor and muscle cell types as a powerful reference platform for future functional and evolutionary neuroscience. Both giant axons and striated muscles may have evolved independently in this lineage (apart from other cnidarians and bilaterians). Thus, Aglantha is an example of "the extreme case" of neuromuscular adaptations driven by the prominent neuronal concentrations in the form of the annulus central nervous system to support the fast escape swimming and other elaborate behavioral repertoire. We also conclude that in Cnidaria the centralization of neural systems might have evolved at least three times in each of the medozozoan lineage (Scyphozoa, Cubozoa, and Hydrozoa).