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J Comp Neurol. 2020 Feb 15;528(3):481-501. doi: 10.1002/cne.24770. Epub 2019 Oct 4.

Comparative neuroanatomy of ctenophores: Neural and muscular systems in Euplokamis dunlapae and related species.

Author information

1
Whitney Laboratory for Marine Bioscience, 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

Ctenophora is an early-branching basal metazoan lineage, which may have evolved neurons and muscles independently from other animals. However, despite the profound diversity among ctenophores, basal neuroanatomical data are limited to representatives of two genera. Here, we describe the organization of neuromuscular systems in eight ctenophore species focusing on Euplokamis dunlapae-the representative of the lineage sister to all other ctenophores. Cydippids (Hormiphora hormiphora and Dryodora glandiformis) and lobates (Bolinopsis infundibulum and Mnemiopsis leidyi) were used as reference platforms to cover both morphological and ecological diversity within the phylum. We show that even with substantial environmental differences, the basal organization of neural systems is conserved among ctenophores. In all species, we detected two distributed neuronal subsystems: the subepithelial polygonal network and the mesogleal elements. Nevertheless, each species developed specific innovations in neural, muscular, and receptor systems. Most notable Euplokamis-specific features are the following: (a) Comb nerves with giant axons. These nerves directly coordinate the rapid escape response bypassing the central integrative structure known as the aboral sensory organ. (b) Neural processes in tentacles along the rows of "boxes" providing structural support and located under striated muscles. (c) Radial muscles that cross the mesoglea and connect the outer wall to the aboral canal. (d) Flat muscles, encircling each meridional canal. Also, we detected a structurally different rectangular neural network in the feeding lobes of Lobata (Mnemiopsis/Bolinopsis) but not in other species. The described lineage-specific innovations can be used for future single-cell atlases of ctenophores and analyses of neuronal evolution in basal metazoans.

KEYWORDS:

Beroe; Ctenophora; F-actin; Mnemiopsis; Pleurobrachia; Stereocilia; apical organ; cell atlas; cilia; development; evolution; mesoglea; microvilli; muscle system; nervous system; phylogeny; receptors; sensory cells; tubulin

PMID:
31498892
DOI:
10.1002/cne.24770

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