Cited by 93Marine Invertebrate Physiology and EcologyMarine Sponges and Natural ProductsDevelopmental Biology and Gene Regulation

Evolutionary emergence of synaptic nervous systems: what can we learn from the non‐synaptic, nerveless Porifera?

Open access
Nickel, Michael·2010·Invertebrate Biology

Abstract

Abstract.The Porifera represent one of the only two recent nerveless and muscleless metazoan phyla. Nevertheless, sponges provide behavioral, physiological, pharmacological, morphological, and, more recently, an increasing amount of genetic evidence for a paracrine pre‐nervous integration system. Although this system might be derived, it allows us to draw conclusions, on the basis of comparative data, about the origin of the nervous systemsensu strictoas found in the eumetazoan phyla. The goal of the present review is to compile recent evidence on the sponge integration systems. Based on this framework, new light is also shed on the evolutionary origin of the eumetazoan synaptic nervous systems, which can be regarded to form an evolutionary biochemical continuum with the paracrine signaling system in sponges. Thus, we can assume that the evolutionary transition from a paracrine‐dominated, pre‐nervous system to an electrochemically dominated, primordial nervous system resulted in part from compartmentalization effects. As intermediate evolutionary stages, regionalized synapse precursor areas might have occurred within pre‐nervous cells, which foreshadowed the highly organized synaptic scaffolds present in recent nerve cells of the Eumetazoa.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1111/j.1744-7410.2010.00193.x

Cites

9 of 9 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • The first synapse arose from the aggregation of vesicle-related intercellular signalling modules, including synaptotagmin, SNARE-complex components and postsynaptic receptor complexes.

    “Similar ideas have been put forward repeatedly [5,66,67] and imply that the first synapse arose from the aggregation of vesicle-related intercellular signalling modules, including synaptotagmin, SNARE-complex components and postsynaptic receptor complexes, as extensively reviewed elsewhere [15,32,34,46,60].”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 26

  1. Bidder GP 1937. The perfection of sponges. Proc. Linn. Soc. London 149: 119-147.
  2. Grundfest H 1959. Evolution of conduction in the nervous system. In: Evolution of Nervous Control from Primi- tive Organisms to Man. Bass A, ed., pp. 43-86. Amer- ican Association for the Advancement of Science, Washington.
  3. FFF 1965. Evolution of electrophysiological varieties among sensory receptor systems. In: Essays on Physio- logical Evolution. Pringle J, ed., pp. 107-138. The Mac- millan Company, New York.
  4. Hanstro¨m B 1928. Vergleichende Anatomie des Nerven- systems der wirbellosen Tiere unter Beru¨cksichtigung seiner Funktion. Springer, Berlin.
  5. FFF 1968. Primitive Nervous Systems. Yale University Press, New Haven. 148 pp.
  6. Leys SP 2007. Sponge coordination, tissues, and the evolution of gastrulation. In: Porifera Reserach: Biodi- versity, Innovation and Sustainability. Custo´dio M, Loˆbo-Hajdu G, Hajdu E, & Muricy G, eds., pp. 53-59. Se´rie Livros 28. Museu Nacional, Rio de Janeiro.
  7. Leys SP, Mackie GO, Reiswig HM, & David WS 2007. The Biology of Glass Sponges. Academic Press. 145 pp.
  8. Leys SP, Nichols SA, & Adams EDM 2009. Epithelia and integration in sponges. Integr. Comp. Biol. (in press).
  9. Lichtneckert R & Reichert H 2007. 1.19 Origin and Evo- lution of the First Nervous System. In: Evolution of Nervous Systems. Volume 1: Theories, Development, Invertebrates. Kaas JH, ed., pp. 289-315. Academic Press, Amsterdam, the Netherlands.
  10. FFF 1979. Is there a conduction system in sponges? In: Biologie des Spongiaires. Editions du C.N.R.S. Le´vi C & Boury-Esnault N, eds., pp. 145-152.
  11. Meech RW & Mackie GO 2007. Evolution of excitability in lower metazoans. In: Invertebrate Neurobiology. North G & Greenspann J, eds., pp. 581-615. Cold Spring Harbor Laboratory Press, New York.
  12. Minchin E 1900. Sponges. In: A Treatise on Zoology. Part II The Porifera and Coelentera. Lancester ER, ed., pp. 1-178.
  13. Nichols SA, Dirks W, Pearse JS, & King N 2006. Early evolution of animal cell signaling and adhesion genes. Proc. Nat. Acad. Sci. USA 103: 12451-12456.
  14. Nickel M 2001. Cell biology and biotechnology of marine invertebrates. Sponges (Porifera) as model organisms. Dissertation, Universita¨t Stuttgart, Stuttgart. 157 pp.
  15. Nickel M, Hammel J, Herzen J, Bullinger E, & Beckmann F 2008. High density resolution synchrotron radiation based x-ray microtomography (SR mCT) for quantita- tive 3D-morphometrics in zoological sciences. Proc. SPIE 70781W, 1-11.
  16. Oberdisse E, Hackenthal E, & Kuschinsky K 1997. Pharmakologie und Toxikologie. Springer-Verlag, Hei- delberg. 770 pp.
  17. Pantin CFA 1952. The elementory nervous system. Proc. Roy. Soc. Lond. Ser. B Biol. Sci. 140: 147-168.
  18. Passano L 1963. Primitive nervous systems. Proc. Nat. Acad. Sci. USA 50: 306-313.
  19. FFF 1979. Cell correlations and integrations in sponges. In: Biologie des Spongiaires. Le´vi C & Boury-Esnault N, eds., pp. 123-135. Editions du CNRS, Paris. FFF 1981. Demonstration of actin filaments in sponge cells. Cell Biol. Int. 5: 945-952.
  20. Ruediger T & Bolz J 2007. Neurotransmitters and the de- velopment of neuronal circuits. In: Axon Growth and Guidance. Bagnard D, ed., pp. 104-115. Series: Ad- vances in Experimental Medicine and Biology Volume 621. Landes Bioscience and Springer Science1Business Media, TX, USA.
  21. Schmidt-Rhaesa A 2007. The Evolution of Organ Systems. Oxford University Press, Oxford.
  22. Sherrington CS 1897. Croonian lecture: The mammalian spinal cord as an organ of reflex action. Proc. Roy. Soc. Lond. 61: 220-221.
  23. Simpson TL 1984. The Cell Biology of Sponges. Springer Verlag, New York. 662 pp.
  24. Steinmetz PRH, Saina M, Amon-Hassenzahl A, Houliston E, Degnan B, & Technau U 2008. An early metazoan origin of striated and smooth muscle cell types. ICREA Conference on the Origin and Early Evolution of Meta- zoans, October 24-25, 2008, Barcelona, Programme: 8.
  25. Thiney Y 1972. Morphologie et cytochimie ultrastructurale de l'oscule d'Hippospongia communis LMK et de sa re´ge´ne´ration. PhD thesis, Universite´Claude Bernard (Lyon I). pp. 1-63.
  26. Zocchi E, Carpaneto A, Cerrano C, Bavestrello G, Giovine M, Bruzzone S, Guida L, Franco L, & Usai C 2001. The temperature-signaling cascade in sponges involves a heat-gated cation channel, abscisic acid, and cyclic ADP-ribose. Proc. Nat. Acad. Sci. USA 98: 14859- 14864.

Cited by

Sorted by citations

Authors
Nickel, M.
Affiliations
Friedrich Schiller University Jena (DE)
Corresponding author
Nickel, Michael
Venue
Invertebrate Biology
Publisher
Wiley
Published
2010-02
Volume
129
Issue
1
Pages
1-16
ISSN
  • 1077-8306 (ISSN-L)
  • 1744-7410
OpenAlex
W2061016427
Cited by
93
References
9
Citations by year
2025: 1 · 2024: 6 · 2023: 5 · 2022: 5 · 2021: 5 · 2020: 6 · 2019: 11 · 2018: 6 · 2017: 7 · 2016: 7 · 2015: 8 · 2014: 7 · 2013: 5 · 2012: 2
FWCI
4.29
Type
journal article
Language
en
Open access
Locations
  • Invertebrate Biology (publishedVersion)
  • Helmholtz Centre for Ocean Research Kiel (GEOMAR) (acceptedVersion)
  • DESY Publication Database (PUBDB) (Deutsches Elektronen-Synchrotron) (submittedVersion, other-oa)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
sponges, paracrine signaling, compartmentalization

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review