Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2015 Feb 15;218(Pt 4):598-611.
doi: 10.1242/jeb.110692.

Convergent Evolution of Neural Systems in Ctenophores

Affiliations
Free PMC article
Review

Convergent Evolution of Neural Systems in Ctenophores

Leonid L Moroz. J Exp Biol. .
Free PMC article

Abstract

Neurons are defined as polarized secretory cells specializing in directional propagation of electrical signals leading to the release of extracellular messengers - features that enable them to transmit information, primarily chemical in nature, beyond their immediate neighbors without affecting all intervening cells en route. Multiple origins of neurons and synapses from different classes of ancestral secretory cells might have occurred more than once during ~600 million years of animal evolution with independent events of nervous system centralization from a common bilaterian/cnidarian ancestor without the bona fide central nervous system. Ctenophores, or comb jellies, represent an example of extensive parallel evolution in neural systems. First, recent genome analyses place ctenophores as a sister group to other animals. Second, ctenophores have a smaller complement of pan-animal genes controlling canonical neurogenic, synaptic, muscle and immune systems, and developmental pathways than most other metazoans. However, comb jellies are carnivorous marine animals with a complex neuromuscular organization and sophisticated patterns of behavior. To sustain these functions, they have evolved a number of unique molecular innovations supporting the hypothesis of massive homoplasies in the organization of integrative and locomotory systems. Third, many bilaterian/cnidarian neuron-specific genes and 'classical' neurotransmitter pathways are either absent or, if present, not expressed in ctenophore neurons (e.g. the bilaterian/cnidarian neurotransmitter, γ-amino butyric acid or GABA, is localized in muscles and presumed bilaterian neuron-specific RNA-binding protein Elav is found in non-neuronal cells). Finally, metabolomic and pharmacological data failed to detect either the presence or any physiological action of serotonin, dopamine, noradrenaline, adrenaline, octopamine, acetylcholine or histamine - consistent with the hypothesis that ctenophore neural systems evolved independently from those in other animals. Glutamate and a diverse range of secretory peptides are first candidates for ctenophore neurotransmitters. Nevertheless, it is expected that other classes of signal and neurogenic molecules would be discovered in ctenophores as the next step to decipher one of the most distinct types of neural organization in the animal kingdom.

Keywords: Ctenophora; Evolution; Genome; Mnemiopsis; Neurons; Neurotransmitters; Phylogeny; Pleurobrachia.

Figures

Fig. 1.
Fig. 1.
Origins of neurons and parallel evolution of neural centralization. A simplified view of evolutionary relationships in the animal kingdom; the tree is combined with the presence or absence of a central nervous system (CNS) or brain in selected animal clades [modified and updated from Moroz (Moroz, 2009; Moroz, 2012; Moroz et al., 2014)]. Choanoflagellates are placed at the base of the tree as a sister group for Metazoa (King et al., 2008) followed by Ctenophora (represented by the photo of Pleurobrachia bachei) as the sister group to all other animals. The image representing the ancestral ctenophore is the fossil known as Eoandromeda (Tang et al., 2011). Porifera and Placozoa do not have recognized neurons. Cnidaria and Ctenophora have well defined neurons and muscles. Although neuronal organization in basal Metazoa can be superficially presented as a nerve net, many species have a prominent concentration of neuronal elements, and numerous and apparently autonomous networks governing surprisingly complex and well coordinated behaviors. Cubozoa have well-developed eyes and a ganglionic organization associated with rhopalia, which can be described in terms of a centralized nervous system in this and other cnidarians (Satterlie, 2011). Similarly, there is a well-defined concentration of neural elements associated with locomotory combs, the aboral organ in Ctenophora. Chordates, nematodes, molluscs and arthropods have well-defined CNSs, whereas in other bilaterians (e.g. phoronids, brachipods, Xenoturbellida, Nemertodermatida) the gross anatomical organization of their nervous systems can be similar or even simpler than those in selected cnidarians and ctenophores. Centralization of nervous systems occurred in parallel within several lineages representing all three major clades in bilaterians (Deuterostomes, Ecdysozoa and Lophotrochozoa). Red numbers indicate that at least nine independent events of neuronal centralization have occurred during evolution. Even in Mollusca, this centralization of the nervous system might occur 4–5 times in parallel (Kocot et al., 2011; Moroz, 2012). Only representative groups of the 34–36 recognized animal phyla are shown in the diagram (Nielsen, 2012). Colored circles indicate possible events of multiple origins of neurons: blue, the origin of neurons in Ctenophores; red, the origin of neurons in Bilateria/Cnidaria clade; it is also possible that some neural populations could originate in bilaterian lineages (yellow, orange and pink circles). This reconstruction of phylogenetic relationships among phyla is a combined view based upon recent large-scale molecular/phylogenomic analyses of several hundred proteins from representatives of more than 15 animal phyla (Hejnol et al., 2009a; Kocot et al., 2011; Moroz et al., 2014; Philippe et al., 2011; Ryan et al., 2013b). The origin of animals can be traced back to about 600 Mya (Erwin et al., 2011; Erwin and Valentine, 2013). However, the extant animal phyla might have more recent evolutionary history. It appears that the origin of major bilaterian groups occurred within a relatively short geological time (probably within 20 million years or even less). As a result the accurate evolutionary relationships among basal lineages and major bilaterian phyla might not be well resolved. Possible timing of the divergence in the diagram is indicated as Mya.
Fig. 2.
Fig. 2.
Neural nets and synapses in ctenophores. (A–D) The basic features of synapses in ctenophores. (A) The generalized asymmetrical synapse. (B) Symmetrical neurite-to-neurite synapse in Beroe. Scale bar: 100 nm. (C) Asymmetrical synapse between a neurite and an epithelial cell (ep) in epidermis of Pleurobrachia. Scale bar: 200 nm. (D) Soma-to-soma reciprocal synapse in the epithelium of Bolina hydatina. Scale bar: 100 nm. c.v., cytoplasmic vesicles; co, dense coat on the postsynaptic membrane; e.r., endoplasmic reticulum; g, Golgi complex; l, intracleft dense line; M, mesoglea; mi, mitochondrion; mt, microtubules; n, nucleus; p, presynaptic dense projections; r, ribosomes; s.v., synaptic vesicle. (E) The schematic diagram of the subepithelial nerve system of a generalized cydippid (the aboral view). Images are reproduced and adapted from Hernandez-Nicaise (Hernandez-Nicaise, 1991) with permission from Wiley-Liss, Inc.
Fig. 3.
Fig. 3.
Neural systems in the ctenophore Pleurobrachia bachei. (A) The subepithelial nerve net as revealed by acetylated β-tubulin immunostaining (L.L.M. and T. P. Norekian, unpublished results). Aboral side is located in the upper part of the photo. (B) The subepithelial net as revealed by tyrosinated α-tubulin immunolabeling (red); blue, nuclear (DAPI) staining; green, phalloidin (actin marker). Note neuronal somata within individual meshes. (C) Neural-type cells in mesoglea; red, tyrosinated α-tubulin immunolabeling; blue, nuclear (DAPI) staining. (D) The distributed neural networks around the mouth of Pleurobrachia. Modified from Moroz (Moroz et al., 2014); green, tyrosinated α-tubulin immunolabeling; red, phalloidin.
Fig. 4.
Fig. 4.
Glutamate and aspartate as neuromuscular transmitter candidates in the ctenophore Pleurobrachia bachei. (A) l-glutamate (0.5–1 mmol l−1) induced action potentials in mechanically isolated muscle cells whereas other transmitter candidates were ineffective even at concentrations up to 5 mmol l−1. Typical responses of ctenophore muscle cells to local pulses of a transmitter application were externally recorded both as individual action potentials and video contractions from a single muscle cell (D). Image modified from Moroz (Moroz et al., 2014); see all details in this paper. (B) The graph shows normalized responses from the same muscle cell indicating l-glutamate is the most potential excitatory molecule compared with d-glutamate or l/d-aspartate. (C) GABA immunolabeling of muscle cells in Pleurobrachia. From Moroz (Moroz et al., 2014) and L.L.M. and T. P. Norekian, unpublished results. Red arrows indicate contractile muscle cells around comb plates; these cells were isolated for electrophysiological tests in A and B. Yellow asterisk marks the base of a single comb plate (polster, see Fig. 2E); red asterisk marks non-contractile muscle fibers possibly involved in cilia beat coordination across the entire comb row. Scale bars: 70 μm (C) and 20 μm (D). Duration of the recording in A is 50 s.

Similar articles

See all similar articles

Cited by 27 articles

See all "Cited by" articles

Publication types

Substances

LinkOut - more resources

Feedback