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Abstract Ctenophores are descendants of an early branching basal metazoan lineage, which may have evolved neurons and muscles independently from other animals.Mnemiopsisis one of the important reference ctenophore species. However, little is known about its neuromuscular organization. Here, we mapped and tracked the development of the neural and muscular elements in the early hatching cydippid larvae, as well as adultMnemiopsis leidyi. The overall development of the neuromuscular system inMnemiopsiswas very similar toPleurobrachia bachei, although inMnemiopsisthe entire process occurred significantly faster. The subepithelial neural cells were observed immediately after hatching. This population consisted of a dozen of separated individual neurons with short neurites. In about 2 days, when their neurites grew significantly longer and connected to their neighbors, they began to form a canonical polygonal subepithelial network. Mesogleal neural elements prominent in all studied adult ctenophores were not detectable inMnemiopsislarvae but were clearly labeled in closely related Lobata speciesBolinopsis infundibulum. Hatched larvae also had putative mechanoreceptors with long stereocilia and approximately two dozen muscle cells. In adultMnemiopsis,the feeding lobes and auricles contained two distinct populations of neurons and neural ensembles that were not observed in other ctenophore lineages and likely represented elaborate neuronal innovations characteristic for the clade Lobata and their lifestyles.
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Comparative neuroanatomy of ctenophores: Neural and muscular systems in Euplokamis dunlapae and related species
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 onEuplokamis dunlapae—the representative of the lineage sister to all other ctenophores. Cydippids (Hormiphora hormiphoraandDryodora glandiformis) and lobates (Bolinopsis infundibulumandMnemiopsis 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 notableEuplokamis‐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.
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- PAR ID:
- 10374608
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Journal of Comparative Neurology
- Volume:
- 528
- Issue:
- 3
- ISSN:
- 0021-9967
- Page Range / eLocation ID:
- p. 481-501
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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