Ctenophores are descendants of one of the earliest branching metazoan lineage with enigmatic nervous systems. The lack of convenient neurogenic molecules and neurotransmitters suggests an extensive parallel evolution and independent origins of neurons and synapses. However, the field lags due to the lack of microanatomical data about the neuro‐muscular systems in this group of animals. Here, using immunohistochemistry and scanning electron microscopy, we describe the organization of both muscular and nervous systems in the sea gooseberry,
Ctenophores are descendants of an early branching basal metazoan lineage, which may have evolved neurons and muscles independently from other animals.
- NSF-PAR ID:
- 10449881
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Journal of Morphology
- Volume:
- 282
- Issue:
- 10
- ISSN:
- 0362-2525
- Page Range / eLocation ID:
- p. 1466-1477
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Pleurobrachia bachei ,Pleurobrachia consists of two subsystems: the subepithelial neural network and the mesogleal net with about 5,000–7,000 neurons combined. Our data revealed the unexpected complexity of neuromuscular organization in this basal metazoan lineage. The anatomical diversity of cell types includes at least nine broad categories of neurons, five families of surface receptors and more than two dozen types of muscle cells as well as regional concentrations of neuronal elements to support ctenophore feeding, complex swimming, escape, and prey capture behaviors. In summary, we recognize more than 80 total morphological cell types. Thus, in terms of cell‐type specification and diversity, ctenophores significantly exceed what we currently know about other prebilaterian groups (placozoan, sponges, and cnidarians), and some basal bilaterians. -
more » « less
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 andDryodora glandiformis ) and lobates (Bolinopsis infundibulum andMnemiopsis 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. -
more » « less
Abstract Although, neurosensory systems might have evolved independently in ctenophores, very little is known about their organization and functions. Most ctenophores are pelagic and deep‐water species and cannot be bred in the laboratory. Thus, it is not surprising that neuroanatomical data are available for only one genus within the group—
Pleurobrachia . Here, using immunohistochemistry and scanning electron microscopy, we describe the organization of two distinct neural subsystems (subepithelial and mesogleal) and the structure of different receptor types in the comb jellyBeroe abyssicola —Beroe , with five receptor types, covers the entire body surface and expands deep into the pharynx. Three types of mesogleal neurons are comparable to the cydippidPleurobrachia . The predatory lifestyle ofBeroe is supported by the extensive development of ciliated and muscular structures including the presence of giant muscles and feeding macrocilia. The obtained cell‐type atlas illustrates different examples of lineage‐specific innovations within these enigmatic marine animals and reveals the remarkable complexity of sensory and effector systems in this clade of basal Metazoa. -
Abstract Innate immunity is an ancient physiological response critical for protecting metazoans from invading pathogens. It is the primary pathogen defense mechanism among invertebrates. While innate immunity has been studied extensively in diverse invertebrate taxa, including mollusks, crustaceans, and cnidarians, this system has not been well characterized in ctenophores. The ctenophores comprise an exclusively marine, non-bilaterian lineage that diverged early during metazoan diversification. The phylogenetic position of ctenophore lineage suggests that characterization of the ctenophore innate immune system will reveal important features associated with the early evolution of the metazoan innate immune system. Here, we review current understanding of the ctenophore immune repertoire and identify innate immunity genes recovered from three ctenophore species. We also isolate and characterize Mnemiopsis leidyi cells that display macrophage-like behavior when challenged with bacteria. Our results indicate that ctenophores possess cells capable of phagocytosing microbes and that two distantly related ctenophores, M. leidyi and Hormiphora californiensis, possess many candidate innate immunity proteins.more » « less
-
more » « less
Cell suspension fluidics, such as flow cytometry (FCS) and fluorescence-activated cell sorting (FACS), facilitates the identification and precise separation of individual cells based on phenotype. Since its introduction, flow cytometry has been used to analyze cell types and cellular processes in diverse non-vertebrate taxa, including cnidarians, molluscs, and arthropods. Ctenophores, which diverged very early from the metazoan stem lineage, have emerged as an informative clade for the study of metazoan cell type evolution. We present standardized methodologies for flow cytometry-mediated identification and analyses of cells from the model ctenophore
Mnemiopsis leidyi that can also be applied to isolate targeted cell populations. Here we focus on the identification and isolation of ctenophore phagocytes. Implementing flow cytometry methods in ctenophores allows for fine scale analyses of fundamental cellular processes conserved broadly across animals, as well as potentially revealing novel cellular phenotypes and behaviors restricted to the ctenophore lineage.
