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J Comp Neurol. 2019 Nov 21. doi: 10.1002/cne.24821. [Epub ahead of print]

Atlas of the neuromuscular system in the Trachymedusa Aglantha digitale: Insights from the advanced hydrozoan.

Author information

1
Whitney Laboratory for Marine Biosciences, University of Florida, St. Augustine, Florida.
2
Friday Harbor Laboratories, University of Washington, Friday Harbor, Washington.
3
Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia.
4
Department of Neuroscience and McKnight Brain Institute, University of Florida, Gainesville, Florida.

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.

KEYWORDS:

Cnidaria; Nematostella; cell atlas; evolution; hydra; muscle system; nematocysts; nervous system; sensory cells

PMID:
31749185
DOI:
10.1002/cne.24821

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