El Mestikawy S., Walln-Mackenzie A., Fortin G. M., Descarries L., Trudeau L. E. (2011). Penny A. M., Wood R., Curtis A., Bowyer F., Tostevin R., Hoffman K. H. (2014). to distant neural processes. B., Meyer A., Santos S. R., Schander C., Moroz L. L., Lieb B., et al. Ctenophore | Types, Characteristics & Adaptations | Britannica Nervous system and senses. One of the largest categories includes genes that are either ctenophore innovations (such as ctenophore-specific secretory peptides); or ctenophore lineage-specific isoforms (such as WntX). government site. Pleurobrachia is a very abundant ctenophore species in the North Pacific Ocean; whereas the closely related P. pileus is found in the Atlantic Ocean. The first fossil ctenophore from the lower Devonian of West Germany, Maintenance of isolated smooth muscle cells of the ctenophore. The first muscles evolved to control the hydroskeleton and feeding/defensive movements, as in extant ctenophores with l-glutamate as one of the neuromuscular transmitters in addition to secretory peptides. The sea gooseberry Pleurobrachia bachei (Fig. As they are soft-bodied, ctenophores are sparsely represented in the rock record. My oldest sister is a sea walnut? Interestingly, a number of predicted peptides are also differentially expressed in embryonic stages, implying their roles in early segregation of developmental potential. Evolution of sodium channels predates the origin of nervous systems in animals, Neuroid conduction and the evolution of conducting tissues. In collaboration with T. R. Gregory (Guelph University, Canada), we screened various ctenophore species using flow cytometry and densitometry, searching for small genome sizes following previously published protocols (DeSalle et al., 2005). Evidence for involvement of Wnt signalling in body polarities, cell proliferation, and the neuro-sensory system in an adult ctenophore, Origin and early evolution of neural circuits for the control of ciliary locomotion, Suspected chemoreceptors in coelenterates and ctenophores. For example, Pleurobrachia has voltage-gated sodium and many potassium channels that were apparently absent in sponges and a greater diversity of aquaporins (water channels) (Papadopoulos and Verkman, 2013) than all other basal metazoans combined. Aronova M. Z., Titova L. K., Kharkeevitch T. A., Tsirulis T. P. (1979). Evolution The Closest Living Relative of the First Animal Has Finally Been Found A debate has been settled over the earliest animal ancestora free-swimming creature with a well-developed nervous. Many ctenophores possess a characteristic cydippid larva that is similar to adult Pleurobrachia (Fig. All 150+ described ctenophore species are carnivorous animals ranging in habitat from tropical to polar seas (Hernandez-Nicaise, 1991; Hyman, 1940; Kozloff, 1990; Mayer, 1912). Omote H., Miyaji T., Juge N., Moriyama Y. FMRFamide immunoreactivity is generally occurring in the nervous systems of coelenterates, Evolution of conduction in the nervous system, Comparative feeding behavior of planktonic ctenophores. From a number of genes encoding transmitter synthesis and degradation, only orthologs of genes distantly related to phenylalanine hydroxylase (PH) are shared between the choanoflagellate Monosiga, the slime mold Dictyostelium and the ctenophore Pleurobrachia. 2013 Society for Integrative and Comparative Biology Annual Meeting. Hejnol A., Obst M., Stamatakis A., Ott M., Rouse G. W., Edgecombe G. D., Martinez P., Bagu J., Bailly X., Jondelius U., et al. Not surprisingly, ctenophores evolved a variety of electrical synapses (Hernandez-Nicaise, 1991; Satterlie and Case, 1978); these gap junctions are encoded by 12 pannexin/innexin genes in the Pleurobrachia genome (Moroz et al., 2014). The aboral organ (it is sometimes less correctly named as the apical organ because there is an analogous structure in bilaterian larvae) is the primary sensory brain-type structure located at the aboral pole of the animal. The lowest threshold was determined for l-glutamate followed by l-aspartate, d-aspartate and d-glutamate (Fig. Glue-based prey capture with unique tentacle/colloblast apparatus has no analogs across the animal kingdom. (2010). (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. Cambrian comb jellies from Utah illuminate the early evolution of (C) Neural-type cells in mesoglea; red, tyrosinated -tubulin immunolabeling; blue, nuclear (DAPI) staining. Structure and activity of the acid-sensing ion channels. Highstein S. M., Holstein G. R., Mann M. A., Rabbitt R. D. (2014). 2D) and classical asymmetrical (highly polarized) synapses (Fig. Evolution: ctenophore genomes and the origin of neurons, Ctenophores of the Atlantic coast of North America. Transmitter phenotypes include very complex packing, uptake (transporters) and inactivation systems, as well as multipart receptor machinery, with several hundred of genes precisely co-expressed in a given neuronal cell type. Using the machine learning NeuroPID tool, we predicted 129 new putative neuropeptide precursors. The emerging new data from ctenophores allow us to revisit two scenarios of neuronal evolution: (1) polygenesis or independent origins of neural systems in ctenophores versus cnidarian/bilaterian clade neurons (Moroz, 2009; Moroz, 2012; Moroz, 2013; Moroz et al., 2014; Moroz et al., 2012; Pennisi, 2013) and (2) monophyly or a single origin of the neural system with massive loss of majority neurotransmitters and some neurogenic molecular components in ctenophores (Rokas, 2013). 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. Some species have developed systems of relatively large neurons and axons (up to ~612 m in diameter) to support fast escape (Mackie et al., 1992) and feeding (Tamm and Tamm, 1995) behaviors. Cnidaria and Ctenophora have well defined neurons and muscles. The presence of many components critical for synaptic function in bilaterians (e.g. Notably, the expression of most of ASSCs is correlated with the morphological appearance of neurons in development, and ASSC expression is most abundant in tentacles, combs and apical organs structures that are highly enriched in neural elements and under complex synaptic control. Most likely, the revealed polygonal lattice results from a growth pattern where each polygon encircles a group of epithelial cells, even in very young larvae (Hernandez-Nicaise, 1991). Conductive elements can be either derivatives of muscles or neurons. the contents by NLM or the National Institutes of Health. A nerve net is a diffuse network of neurons that sends impulses all over from one point of stimuli. (C) Asymmetrical synapse between a neurite and an epithelial cell (ep) in epidermis of Pleurobrachia. These data suggest both well-developed glutamate signaling and its remarkable parallel evolution in ctenophores. Yes, these genes are equally critical for many other non-neuronal functions; and, in bilaterians, they are also expressed in a diversity of non-neuronal tissues. consistent with a shared ancestry of nervous systems. The first proto-neurons could mediate their action via volume transmission without structurally differentiated synapses. Definition of ctenophores in the Definitions.net dictionary. Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes. Primary central nervous system lymphoma - Nature The results of Pleurobrachia whole-genome sequencing were formally reported at the SICB meeting in Charleston (SC) in January 2012 (Moroz et al., 2012), suggesting convergent evolution of ctenophore neural systems. (2011). In summary, we know very little about ctenophore neural organization; and virtually nothing about the cellular or transmitter bases of their behaviors. The presynaptic component is usually interpretable as a nerve fiber, but realistic synapses have also been found with a muscle cell as the presynaptic element (Horridge, 1974). Aquaporin water channels in the nervous system. Therefore, they can not be considered as unique synaptic markers, even in bilaterians. Deep metazoan phylogeny: when different genes tell different stories. The study of neural organization by Hertwig (Hertwig, 1880) was a logical expansion of the similar studies on cnidarians by Hertwig's brothers (Hertwig and Hertwig, 1878; Hertwig and Hertwig, 1879; Hertwig and Hertwig, 1880). As ctenophores possess an elaborate and centralized nervous system (contrary to poriferans), this radically changes current perspectives on the early evolution of neurons and nervous systems and raises a number of possibilities with regard to the evolutionary origin (s) of neurons. Schnitzler C. E., Pang K., Powers M. L., Reitzel A. M., Ryan J. F., Simmons D., Tada T., Park M., Gupta J., Brooks S. Y., et al. No genes encoding enzymes for synthesis of acetylcholine (i.e. Several of these ctenophore-specific precursors are expressed in polarized cells around the mouth, in tentacles and polar fields (e.g. A., Kirkness E. F., Simakov O., Hampson S. E., Mitros T., Weinmaier T., Rattei T., Balasubramanian P. G., Borman J., Busam D., et al. Finding a rare fossilized comb jelly reveals new gaps in the fossil record The non-cydippid body plan of Mnemiopsis and Bolinopsis can be derived from a cydippid body plan of Pleurobrachia. secretory apparatus, receptors, ion channels, etc.) The majority of cnidarians do not possess true muscle cells they have so-called epitheliomuscular cells with mixed features of epithelial and contractive cells (Brusca and Brusca, 2003). Note neuronal somata within individual meshes. Nevertheless, excitatory and inhibitory inputs on different effectors (cilia, tentacles, muscles, colloblasts, etc.) These prohormone-derived peptides could have a variety of functions including cell-to-cell signaling, toxins or involvement in innate immunity, or a combination of all three. "For a long time, it was assumed. For more than a century, ctenophores and cnidarians were superficially united as jelly-like diploblastic organisms with the simplest tissue organization derived from two embryonic layers (ectoderm and endoderm). Image modified from Moroz (Moroz et al., 2014); see all details in this paper. These neuroid elements (possible muscle-derived with electrical synapses between cells) operate in parallel to synapse-based neural systems. But their mostly see-through bodies cloak a nervous system unlike that of any other known. A., Chen J., Askwith C. C., Hruska-Hageman A. M., Price M. P., Nolan B. C., Yoder P. G., Lamani E., Hoshi T., Freeman J. H., Jr, et al. All described interneuronal and neuro-effector chemical synapses in all ctenophores have unique organization (Fig. Neural systems in the ctenophore Pleurobrachia bachei. Next, we used direct ultrasensitive microchemical assays [capillary electrophoresis with different detection schemes from femtomolar (1015) to attomolar (1018) limits of detection (see Fuller et al., 1998; Moroz et al., 2005)] to look for canonical low molecular weight (neuro)transmitter candidates in four species Pleurobrachia bachei, Mnemiopsis leidy, Bolinopsis infundibulum and Beroe abyssicola. Resolving the metazoan tree of life with advanced bioinformatic pipelines and phylogenetic methods, http://www.sicb.org/meetings/2013/schedule/abstractdetails.php?id=235, http://www.sicb.org/meetings/2015/schedule/abstractdetails.php?id=466, http://sicb.org/meetings/2012/schedule/abstractdetails.php?id=527, http://www.sicb.org/meetings/2013/schedule/abstractdetails.php?id=1280, www.sicb.org/meetings/2015/schedule/abstractdetails.php?id=851. The gravity receptor, [Electronmicroscopic study of the gravity receptors in ctenophores]. King N., Westbrook M. J., Young S. L., Kuo A., Abedin M., Chapman J., Fairclough S., Hellsten U., Isogai Y., Letunic I., et al. Lentz, 1968; Mackie, 1970; Mackie, 1990; Miller, 2009; Moroz, 2009; Parker, 1919; Sakharov, 1974) and recently (Marlow and Arendt, 2014; Moroz, 2014; Moroz et al., 2014), I will emphasize the alternative polygenesis scenario in this communication. There is a possibility that the last common ancestor of extant ctenophores shared neuronal toolkits with other eumetazoans (Cnidaria and Bilateria) but this scenario, regardless of phylogenetic reconstructions (Moroz, 2014), still implies a situation whereby modern ctenophores developed a very distinct molecular make-up and lost(?) 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. Ctenophora is an early-branching basal metazoan lineage, which may have evolved neurons and muscles independently from other animals. Other bona fide animals, however, such as jellyfish, sea anemones, sponges and ctenophores, have simpler body plans. (2004). Using capillary electrophoresis, we detected l/d-glutamate and l/d-aspartate as well as -aminobutyric acid (GABA) in all four ctenophore species investigated (Pleurobrachia, Beroe, Bolinopsis, and Mnemiopsis) (Moroz et al., 2014). Glutamate and a diversity of secretory peptides are candidates for ctenophore transmitters. The activity of cilia is under control of the aboral organ composed of several cell types with gravity sensors and a statolith consisting of about 100 lithocytes (Tamm, 1973; Tamm, 1982). The hidden biology of sponges and comb jellies. Could neurons evolve more than once? Since this structure serves both digestive and circulatory functions, it is known as a gastrovascular cavity. However, the extant animal phyla might have more recent evolutionary history. The presence of P2X receptors encoded in ctenophore genomes (Moroz et al., 2014) suggest that purinergic (ATP/ADP-mediated) transmission might occur in ctenophores. Early animal evolution: a morphologist's view - Royal Society Convergent evolution of neural systems in ctenophores - PMC The corollary for such hypotheses would be multiple origins of synapses as well. Broad phylogenomic sampling improves resolution of the animal tree of life, Possible ctenophoran affinities of the Precambrian sea-pen. Centralization of nervous systems occurred in parallel within several lineages representing all three major clades in bilaterians (Deuterostomes, Ecdysozoa and Lophotrochozoa). We do not find any pannexins in choanoflagellates or other basal eukaryotic groups (see also Abascal and Zardoya, 2013; Panchin, 2005), suggesting that these are metazoan innovations with major expansion of this family in the ctenophore lineage. Sherwood T. W., Frey E. N., Askwith C. C. (2012). Regardless of evolutionary interpretations, the sequenced Pleurobrachia genome, combined genomic, metabolomic and physiological data on 10 different species revealed extraordinary and unique molecular diversity of developmental and neural signaling pathways. As such, multiple origins of neurons from different classes of secretory cells might occur more than once during ~600 million years of animal evolution a part of transition from temporal to spatial differentiation (Mikhailov et al., 2009). Genetics. National Library of Medicine Comb jellies have a bizarre nervous system unlike any other animal Erwin D. H., Laflamme M., Tweedt S. M., Sperling E. A., Pisani D., Peterson K. J. Nervous System of . For example, ctenophores have the most sophisticated system of ciliated locomotion in the animal kingdom. Origins of neurons and parallel evolution of neural centralization. The majority of synthetic genes for neurotransmitter pathways are also not present in sequenced unicellular eukaryotes (such as Monosiga and Capsaspora recognized as sister groups for animals) suggesting they are cnidarian/bilaterian innovations. Comb jellies' unique fused neurons challenge evolution ideas - Nature Gap junctions suggest epithelial conduction within the comb plates of the ctenophore. Polarized secretory cells might not be genetically or developmentally related to neurons. The ctenophore genome and the evolutionary origins of neural - Nature Thus, ctenophores have the most dissimilar transmitter organization among all animals studied so far (see Kohn and Moroz, 2015b). The ciliated locomotion mode itself can be viewed as a primordial mode of movements mediated by specialized ctenes or the combs, organized in eight rows of comb plates. are eliminated by elevated levels of Mg2+, suggesting the presence of directional neural circuits with functional chemical synapses (Horridge, 1974; Tamm, 1982). 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)]. Indeed, the GABA transaminase gene, also found in the Pleurobrachia genome, encodes the enzyme that catalyses the conversion of GABA back into succinic semialdehyde and glutamate following formation of succinic acid that enters the citric acid cycle the universal aerobic bioenergetics pathway. open access Highlights Keywords ctenophores sponges comparative biology genomics morphology Viewing all animals through a bilaterian lens distorts the view of animal evolution We have two windows on early animal evolution: fossils and living animal diversity. Hernandez-Nicaise M. L., Amsellem J. First, it is one of the earliest lineages of pre-bilaterian animals possessing true nervous systems and mesoderm-derived muscles. Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Ctenophora - an overview | ScienceDirect Topics Schierwater B., Eitel M., Jakob W., Osigus H. J., Hadrys H., Dellaporta S. L., Kolokotronis S. O., Desalle R. (2009). What does ctenophores mean? - Definitions.net (A) l-glutamate (0.51 mmol l1) induced action potentials in mechanically isolated muscle cells whereas other transmitter candidates were ineffective even at concentrations up to 5 mmol l1. 1). However, and in contrast to observations of all other animals with nervous systems, several genes controlling neuronal fate and patterning, such as neurogenins, NeuroD, AchaeteScute, REST and HOX/otx, are absent in the ctenophores we sampled (Moroz et al., 2014). Yet, as our capillary electrophoresis data suggest, these PH-related enzymes, if functional, do not produce any known catecholamines in ctenophores. However, I would not exclude the presence of other small signal molecules, including those with no analogs in other metazoans. The research was supported by National Science Foundation Synaptic vesicles are apparently very diverse at the ultrastructural level, suggesting the presence of multiple low molecular weight and neuropeptide-type transmitters of unknown identity. Philippe H., Derelle R., Lopez P., Pick K., Borchiellini C., Boury-Esnault N., Vacelet J., Renard E., Houliston E., Quinnec E., et al. It is a bold hypothesis since the nervous system is a very . 8600 Rockville Pike Comparative neuroanatomy of ctenophores: Neural and muscular - PubMed A., Hecht E. E., Hof P. R., et al. The role of l-glutamate as an intercellular messenger is supported by an unprecedented diversity of ionotropic glutamate receptors, iGluR, in the Pleurobrachia genome and 10 other ctenophores we examined, including Mnemiopsis (Moroz et al., 2014). Fuller R. R., Moroz L. L., Gillette R., Sweedler J. V. (1998). Schnitzler C. E., Simmons D. K., Pang K., Martindale M. Q., Baxevanis A. D. (2014). Whether peptide- or proton-mediated (neuro)transmission exists in ctenophores is a subject for future studies. Assessing the root of bilaterian animals with scalable phylogenomic methods. Even if a candidate compound was not detected, we still performed extensive pharmacological screening for potential behavioral effects using semi-intact preparations with exposed ciliated combs (to be sure that the pharmacological agent gained access to the nervous system) and isolated muscle. If true, it could mean that many of the traits ctenophores share with typical animals (such as a nervous system, gut and complex muscles) might have evolved twice: once in comb jellies and . We have brains that send messages almost instantly throughout the body through a connection of nerves, they do not have that. In fact, ctenophore neurons are very elusive cells to stain with convenient histological dyes. Modified from Moroz (Moroz et al., 2014); green, tyrosinated -tubulin immunolabeling; red, phalloidin. The pacific lobate Bolinopsis infundibulum has the second smallest genome (~220 Mb) whereas Beroe abyssicola has one of the largest genomes within the group: ~1 Gb. Ctenophores and the evolutionary origin (s) of neurons This statement still holds true today and we know nothing about any functional neural circuit in ctenophores. Finally, protons, ATP and related nucleotides as well as gaseous molecules such as NO, H2S and CO might also be recruited as intercellular messengers early in evolution. Did the ctenophore nervous system evolve independently? The phylogenetic position of ctenophores and the origin(s) of nervous As ctenophores possess an elaborate and centralized nervous system (contrary to poriferans), this radically changes current perspectives on the early evolution of neurons and nervous systems and raises a number of possibilities with regard to the evolutionary origin (s) of neurons. Ctenophores evolved arrays of multiciliated cells supporting their highly efficient mode of locomotion. Ryan J. F., Pang K., Schnitzler C. E., Koch B. J., Nguyen A.-D., Moreland R. T., Mullikin J. C., Wolfsberg T. G., Martindale M. Q., Baxevanis A. D. (2013a). 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. Furthermore, acetylcholine, classical catecholamines (dopamine, noradrenaline, adrenaline), serotonin and histamine were not detected in ctenophores using direct microchemical assays (Moroz et al., 2014). Chen J. Y., Bergstrom J., Lindstrom M., Hou X. G. (1991). Some phylogenomic analyses support Porifera as the sister group to all other animals ().There is growing evidence, however, that Ctenophora is the sister group to all other animals (8, 9).The latter indicates that some nervous system features arose independently in ctenophores or . This pioneered work was challenged but later reproduced by Driesch and Morgan (Driesch and Morgan, 1895). Second, we also found that orthologs of bilaterian and cnidarian pan-neuronal markers are not expressed in ctenophore neurons, suggesting that they perform different functions. 1). 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. The phylogeny revealed surprising relationships within ctenophores, with multiple examples of mosaic evolution, such as loss of cydippid larval stages consistent with earlier reconstructions using 18S rRNAs (Podar et al., 2001).