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Cnidarians and the evolutionary origin of the nervous system
Open accessAbstract
Cnidarians are widely regarded as one of the first organisms in animal evolution possessing a nervous system. Conventional histological and electrophysiological studies have revealed a considerable degree of complexity of the cnidarian nervous system. Thanks to expressed sequence tags and genome projects and the availability of functional assay systems in cnidarians, this simple nervous system is now genetically accessible and becomes particularly valuable for understanding the origin and evolution of the genetic control mechanisms underlying its development. In the present review, the anatomical and physiological features of the cnidarian nervous system and the interesting parallels in neurodevelopmental mechanisms between Cnidaria and Bilateria are discussed.
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“Though at least 600 million years of evolution separate cnidarians from bilaterians [9–16], many aspects of the nervous system are conserved, including neuropeptides and neurotransmitters [15–20].”
From The Jellyfish Cassiopea Exhibits a Sleep-like State (2017) · cites this paper as [18]
In the citing paper
“The publication of several cnidarian genomes has shown that much of the molecular architecture underlying neurogenesis and neuron functioning is conserved between bilaterians and cnidarians [17,47–51].”
From Evolution of eumetazoan nervous systems: insights from cnidarians (2015) · cites this paper as [51]
In the citing paper
“Nerve net-like arrangements of neurons cover the almost entire ectoderm in cnidarians and ctenophores [61,129,130–136].”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [136]
In the citing paper
“The presence of a well-developed nerve net correlates with the presence of basiepithelial muscle fibres directly innervated by nerve net neurons, in cnidarians and in ctenophores [61,67,128,132,133,135,136,138–142].”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [136]
In the citing paper
“In the cerianthids, a basal cnidarian lineage, the nerve net appears to be of purely ectodermal nature [128], which suggests that the evolution of inner layer neurons occurred independently in ctenophore, cnidarian and bilaterian lineages [136].”
From Gastric pouches and the mucociliary sole: setting the stage for nervous system evolution (2015) · cites this paper as [136]
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“It has already been shown that some neural bHLH transcription factors are expressed in developing neurons in hydrozoans (Grens et al., 1995; Seipel et al., 2004; reviewed in Watanabe et al., 2009).”
BackgroundInfluentialGenomics and development of Nematostella vectensis and other anthozoans
Rentzsch, F., & Technau, U. (2016) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2016.05.024 · Cited by 32
Effect of neurotoxic compounds on ephyrae of Aurelia aurita jellyfish
Costa, E., Gambardella, C., Piazza, V., Greco, G., Lavorano, S., Beltrandi, M., Bongiovanni, E., Gnone, G., Faimali, M., & Garaventa, F. (2015) · Hydrobiologia · doi:10.1007/s10750-015-2284-3 · Cited by 34
“Moreover, a role of neuronal control has been proved to regulate the periodic contractions of A. aurita body, in order to generate ring-vortices of the surrounding medium (Satterlie, 2002; Watanabe et al., 2009).”
BackgroundResultA myxozoan genome reveals mosaic evolution in a parasitic cnidarian
Guo, Q., Atkinson, S. D., Xiao, B., Zhai, Y., Bartholomew, J. L., & Gu, Z. (2022) · BMC Biology · doi:10.1186/s12915-022-01249-8 · Cited by 31
“Primitive nervous system? While free-living cnidarians have simple nerve nets [85], there is no evidence that similar nerves are present in myxozoans even though they can sense proximity of hosts and can have motile, multi-cellular stages [56].”
BackgroundBusengdal, H., & Rentzsch, F. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.08.021 · Cited by 35
A new look at the architecture and dynamics of the Hydra nerve net
Keramidioti, A., Schneid, S., Busse, C., von Laue, C. C., Bertulat, B., Salvenmoser, W., Heß, M., Alexandrova, O., Glauber, K. M., Steele, R. E., et al. (2023) · eLife · doi:10.7554/elife.87330.3 · Cited by 34
Self-citationEvolution of the Pax-Six-Eya-Dach network: the calcisponge case study
Fortunato, S., Leininger, S., & Adamska, M. (2014) · EvoDevo · doi:10.1186/2041-9139-5-23 · Cited by 32
“ciliatum express SoxB [24], a transcription factor involved in bilaterian neurogenesis [34,35] and expressed in cnidarian neurosensory cells [36].”
BackgroundPhylostratigraphic Profiles in Zebrafish Uncover Chordate Origins of the Vertebrate Brain
Šestak, M. S., & Domazet‐Lošo, T. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu319 · Cited by 29
“These increases might be expected, given that the first nervous system emerged in this evolutionary range (Koizumi 2007; SchmidtRhaesa 2007; Galliot et al. 2009; Watanabe et al. 2009).”
BackgroundFortunato, S. A. V., Adamski, M., & Adamska, M. (2015) · Marine Genomics · doi:10.1016/j.margen.2015.07.008 · Cited by 31
Zieger, E., & Schubert, M. (2016) · International review of cytology · doi:10.1016/bs.ircmb.2016.09.001 · Cited by 32
Insights into the evolution of digestive systems from studies of Trichoplax adhaerens
Smith, C. L., & Mayorova, T. D. (2019) · Cell and Tissue Research · doi:10.1007/s00441-019-03057-z · Cited by 29
Organization of the ectodermal nervous structures in jellyfish: scyphomedusae
Satterlie, R. A., & Eichinger, J. M. (2014) · The Biological Bulletin · doi:10.1086/bblv226n1p29 · Cited by 30
“In a more general sense, various forms of tubulin antibodies have been used to stain neurons in cnidarians (Groger and Schmid, 2001; Galliot et al., 2009; Watanabe et al., 2009; Nakanishi et al., 2009, 2010), as have RFamide antibodies (Grimmelikhuijzen et al., 1996, 2002).”
BackgroundEv, R., & Raikova, O. I. (2015) · Zoology · doi:10.1016/j.zool.2015.11.004 · Cited by 30
Formery, L., Orange, F., Formery, A., Yaguchi, S., Lowe, C. J., Schubert, M., & Croce, J. C. (2020) · The Journal of Comparative Neurology · doi:10.1002/cne.25012 · Cited by 30
Cephalopods: Ambassadors for rethinking cognition
Schnell, A. K., & Clayton, N. S. (2021) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.12.062 · Cited by 33
Do epidermal keratinocytes have sensory and information processing systems?
Denda, M., & Nakanishi, S. (2021) · Experimental Dermatology · doi:10.1111/exd.14494 · Cited by 31
Tournière, O., Gahan, J. M., Busengdal, H., Bartsch, N., & Rentzsch, F. (2022) · Science Advances · doi:10.1126/sciadv.abi7109 · Cited by 25
Hydraulic and electric control of cell spheroids
Duclut, C., Prost, J., & Jülicher, F. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2021972118 · Cited by 26
The synapsin gene family in basal chordates: evolutionary perspectives in metazoans
Candiani, S., Moronti, L., Pennati, R., de Bernardi, F. L., Benfenati, F., & Pestarino, M. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-32 · Cited by 28
“Thus, the emergence of E domain appears to be correlated with the beginning of the genesis of nervous organization, since the simplest metazoans known to possess a nervous system are those of the phylum Cnidaria [39].”
Hou, X., Qin, Z., Wei, M., Fu, Z., Liu, R., Lu, L., Bai, S., Ma, Y., & Zhang, Z. (2020) · BMC Genomics · doi:10.1186/s12864-020-07312-4 · Cited by 25
Structure and evolution of neuronal wiring receptors and ligands
Cortés, E. C., Pak, J. S., & Özkan, E. (2022) · Developmental Dynamics · doi:10.1002/dvdy.512 · Cited by 25
“DCC homologs have been identified in bilaterians as common receptors that guide commissural projections but are also present in cnidarians(15): For example, the anthozoan model organism Nematostella vectensis (starlet sea anemone) is known to have a complete set of Netrin, DCC, and Unc5-like proteins.(15) In vertebrat…”
BackgroundMedusa: A Review of an Ancient Cnidarian Body Form
Ames, C. L. (2018) · Results and problems in cell differentiation · doi:10.1007/978-3-319-92486-1_7 · Cited by 27
Oren, M., Brickner, I., Appelbaum, L., & Levy, O. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093832 · Cited by 24
“The first appearance of functional nervous systems in animal evolution is attributed to the coelenterates, including the ctenophores (comb jellies) and the cnidarians [5].”
BackgroundTran, C., & Hadfield, M. G. . (2012) · Biological Bulletin · doi:10.1086/bblv222n2p128 · Cited by 24
Cnidarian Nerve Nets and Neuromuscular Efficiency
Satterlie, R. A. (2015) · Integrative and Comparative Biology · doi:10.1093/icb/icv067 · Cited by 25
Clark, E., Kanauchi, D., Kano, T., Aonuma, H., Briggs, D. E. G., & Ishiguro, A. (2018) · Journal of Experimental Biology · doi:10.1242/jeb.192104 · Cited by 22
“Other examples of decentralized nervous control in the animal kingdom include the diffused nerve nets of cnidarians (Watanabe et al., 2009) and other bilaterians such as xenacoelomorphs and hemichordates (Martín-Durán et al.”
BackgroundCapasso, L., Ganot, P., Planas-Bielsa, V., Tambutté, S., & Zoccola, D. (2021) · BMC Molecular and Cell Biology · doi:10.1186/s12860-021-00353-x · Cited by 20
Wong, E., Mölter, J., Anggono, V., Degnan, B. M., & Degnan, B. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-51282-x · Cited by 20
PHYRN: A Robust Method for Phylogenetic Analysis of Highly Divergent Sequences
Bhardwaj, G., Ko, K. D., Hong, Y., Zhang, Z., Ho, N. L., Chintapalli, S. V., Kline, L. A., Gotlin, M. J., Hartranft, D. N., Patterson, M. E., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034261 · Cited by 17
“580 million years ago), which are some of the first organisms known to have a developed neural net, radial axis of symmetry, muscle cells, and stem cells [49,50].”
BackgroundSizemore, T. R., Jonaitis, J., & Dacks, A. M. (2023) · Nature Communications · doi:10.1038/s41467-023-41012-3 · Cited by 21
“isons test was used to determine if: (1) MIPergic LNs preferentially innervate based on the functional group found along the odorant that activates the given glomerulus’ odorant receptor; (2) SPR-GAL4::VP16 expression in antennae and maxillary palps significantly differs between males, mated females, and virgin female…”
Zheng, Y., Cong, X., Liu, H., Wang, Y., Storey, K. B., & Chen, M. (2022) · Biology · doi:10.3390/biology11101538 · Cited by 16
Extracellular matrix and morphogenesis in cnidarians: a tightly knit relationship
Bergheim, B. G., & Özbek, S. (2019) · Essays in Biochemistry · doi:10.1042/ebc20190021 · Cited by 16
Melatonin Distribution Reveals Clues to Its Biological Significance in Basal Metazoans
Roopin, M., & Levy, O. (2012) · PLoS ONE · doi:10.1371/journal.pone.0052266 · Cited by 16
“Although a complete understanding of the cnidarian nervous system has not been obtained, potentially centralized elements, such as circular nerve ring structures, are believed to represent complex features of these presumably simple systems (reviewed in [50]) and have been demonstrated to functionally coordinate a wid…”
BackgroundTranscriptional characterisation of the Exaiptasia pallida pedal disc
Davey, P. A., Rodrigues, M., Clarke, J., & Aldred, N. (2019) · BMC Genomics · doi:10.1186/s12864-019-5917-5 · Cited by 18
Nielsen, S. K. D., Koch, T. L., Wiisbye, S. H., Grimmelikhuijzen, C. J. P., & Garm, A. L. (2021) · The Journal of Comparative Neurology · doi:10.1002/cne.25133 · Cited by 14
“…nature of the neuronal inducers among cnidarians is still unclear, and increased knowledge here would provide important insights not only into the evolutionary origin of neural induction but also into the molecular evolution of the centralized nervous system in bilaterians (Watanabe et al., 2009).”
BackgroundB., L. Q. I., Bartsch, N., Kouzel, I. U., Busengdal, H., Richards, G. S., Steinmetz, P. R. H., & Rentzsch, F. (2023) · Nature Communications · doi:10.1038/s41467-023-39789-4 · Cited by 13
Reconciling Ontic and Epistemic Constraints on Mechanistic Explanation, Epistemically
van Eck, D. (2014) · Axiomathes · doi:10.1007/s10516-014-9243-x · Cited by 14
Zhang, R., Jin, L., Zhang, N., Petridis, A. K., Eckert, T., Scheiner‐Bobis, G., Bergmann, M., Scheidig, A. J., Schauer, R., Yan, M., et al. (2019) · Marine Drugs · doi:10.3390/md17080469 · Cited by 13
“Sialic acid molecules which play also a crucial role in developmental processes [90,91] were invented during the evolution in Echinodermata (e.”
BackgroundNoro, Y., Shimizu, H., Mineta, K., & Gojobori, T. (2021) · Scientific Reports · doi:10.1038/s41598-021-89325-x · Cited by 15
Human transcriptome nexuses: Basic-eukaryotic and metazoan
Vinogradov, A. E. (2010) · Genomics · doi:10.1016/j.ygeno.2010.03.004 · Cited by 14
“The nervous system originated very early in the evolution of metazoans, just after the divergence of sponge and eumetazoan lineages [38,39].”
BackgroundThe histology of Nanomia bijuga (Hydrozoa: Siphonophora)
Church, S. H., Siebert, S., Bhattacharyya, P., & Dunn, C. W. (2015) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22629 · Cited by 14
Metadata
- Authors
- Watanabe, H., Fujisawa, T., & Holstein, T. W.
- Affiliations
- Heidelberg University (DE)
- Corresponding author
- Watanabe, Hiroshi
- Holstein, Thomas W.
- Venue
- Development, Growth & Differentiation
- Publisher
- Wiley
- Published
- 2009-03-30
- Volume
- 51
- Issue
- 3
- Pages
- 167-183
- ISSN
- 0012-1592 (ISSN-L)
- 1440-169X
- OpenAlex
- W1636647670
- Cited by
- 206
- References
- 191
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 16 · 2023: 9 · 2022: 16 · 2021: 26 · 2020: 13 · 2019: 17 · 2018: 7 · 2017: 8 · 2016: 10 · 2015: 19 · 2014: 15 · 2013: 5 · 2012: 8
- FWCI
- 0.96
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Development Growth & Differentiation (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Alexander von Humboldt-Stiftung
- Toyobo Biotechnology Foundation
- Deutsche Forschungsgemeinschaft (SFB 488)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Marine Invertebrate Physiology and Ecology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- Cnidaria, nervous system evolution, brain development, Bilateria, comparative neuroanatomy
- MeSH terms
- Animals, Cnidaria, Biological Evolution, Nervous System, Phylogeny
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