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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.

Nitric oxide (NO) is a ubiquitous gaseous messenger, but we know little about its early evolution. Here, we analyzed NO synthases (NOS) in four different species of placozoans—one of the early-branching animal lineages. In contrast to other invertebrates studied,TrichoplaxandHoilungiahave three distinct NOS genes, including PDZ domain-containing NOS. Using ultra-sensitive capillary electrophoresis assays, we quantified nitrites (products of NO oxidation) andl-citrulline (co-product of NO synthesis froml-arginine), which were affected by NOS inhibitors confirming the presence of functional enzymes inTrichoplax. Using fluorescent single-molecule in situ hybridization, we showed that distinct NOSs are expressed in different subpopulations of cells, with a noticeable distribution close to the edge regions ofTrichoplax. These data suggest both the compartmentalized release of NO and a greater diversity of cell types in placozoans than anticipated. NO receptor machinery includes both canonical and novel NIT-domain containing soluble guanylate cyclases as putative NO/nitrite/nitrate sensors. Thus, althoughTrichoplaxandHoilungiaexemplify the morphologically simplest free-living animals, the complexity of NO-cGMP-mediated signaling in Placozoa is greater to those in vertebrates. This situation illuminates multiple lineage-specific diversifications of NOSs and NO/nitrite/nitrate sensors from the common ancestor of Metazoa and the preservation of conservative NOS architecture from prokaryotic ancestors.

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 hydromedusaAglantha digitaleis 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 inAglantha, 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 inAglanthawith 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 theAglanthalineage (including giant axons innervating striated muscles) strongly support an extensive and wide‐spread parallel evolution of integrative and effector systems across Metazoa.

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.