Skip to main content
NCBI home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2000 Jun 7;267(1448):1071–1079. doi: 10.1098/rspb.2000.1111

The evolution of the serotonergic nervous system.

A Hay-Schmidt 1
PMCID: PMC1690648  PMID: 10885511

Abstract

The pattern of development of the serotonergic nervous system is described from the larvae of ctenophores, platyhelminths, nemerteans, entoprocts, ectoprocts (bryozoans), molluscs, polychaetes, brachiopods, phoronids, echinoderms, enteropneusts and lampreys. The larval brain (apical ganglion) of spiralian protostomes (except nermerteans) generally has three serotonergic neurons and the lateral pair always innervates the ciliary band of the prototroch. In contrast, brachiopods, phoronids, echinoderms and enteropneusts have numerous serotonergic neurons in the apical ganglion from which the ciliary band is innervated. This pattern of development is much like the pattern seen in lamprey embryos and larvae, which leads the author to conclude that the serotonergic raphe system found in vertebrates originated in the larval brain of deuterostome invertebrates. Further, the neural tube of chordates appears to be derived, at least in part, from the ciliary band of deuterostome invertebrate larvae. The evidence shows no sign of a shift in the dorsal ventral orientation within the line leading to the chordates.

Full Text

The Full Text of this article is available as a PDF (745.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adoutte A., Balavoine G., Lartillot N., de Rosa R. Animal evolution. The end of the intermediate taxa? Trends Genet. 1999 Mar;15(3):104–108. doi: 10.1016/s0168-9525(98)01671-0. [DOI] [PubMed] [Google Scholar]
  2. Arendt D., Nübler-Jung K. Comparison of early nerve cord development in insects and vertebrates. Development. 1999 Jun;126(11):2309–2325. doi: 10.1242/dev.126.11.2309. [DOI] [PubMed] [Google Scholar]
  3. Azzaria M., Goszczynski B., Chung M. A., Kalb J. M., McGhee J. D. A fork head/HNF-3 homolog expressed in the pharynx and intestine of the Caenorhabditis elegans embryo. Dev Biol. 1996 Sep 15;178(2):289–303. doi: 10.1006/dbio.1996.0219. [DOI] [PubMed] [Google Scholar]
  4. Cohen B. L., Stark S., Gawthrop A. B., Burke M. E., Thayer C. W. Comparison of articulate brachiopod nuclear and mitochondrial gene trees leads to a clade-based redefinition of protostomes (Protostomozoa) and deuterostomes (Deuterostomozoa) Proc Biol Sci. 1998 Mar 22;265(1395):475–482. doi: 10.1098/rspb.1998.0319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Corbo J. C., Erives A., Di Gregorio A., Chang A., Levine M. Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate. Development. 1997 Jun;124(12):2335–2344. doi: 10.1242/dev.124.12.2335. [DOI] [PubMed] [Google Scholar]
  6. Diefenbach T. J., Sloley B. D., Goldberg J. I. Neurite branch development of an identified serotonergic neuron from embryonic Helisoma: evidence for autoregulation by serotonin. Dev Biol. 1995 Jan;167(1):282–293. doi: 10.1006/dbio.1995.1023. [DOI] [PubMed] [Google Scholar]
  7. Ekström P., Nyberg L., van Veen T. Ontogenetic development of serotoninergic neurons in the brain of a teleost, the three-spined stickleback. An immunohistochemical analysis. Brain Res. 1985 Jan;349(1-2):209–224. doi: 10.1016/0165-3806(85)90145-2. [DOI] [PubMed] [Google Scholar]
  8. Field K. G., Olsen G. J., Lane D. J., Giovannoni S. J., Ghiselin M. T., Raff E. C., Pace N. R., Raff R. A. Molecular phylogeny of the animal kingdom. Science. 1988 Feb 12;239(4841 Pt 1):748–753. doi: 10.1126/science.3277277. [DOI] [PubMed] [Google Scholar]
  9. Halanych K. M., Bacheller J. D., Aguinaldo A. M., Liva S. M., Hillis D. M., Lake J. A. Evidence from 18S ribosomal DNA that the lophophorates are protostome animals. Science. 1995 Mar 17;267(5204):1641–1643. doi: 10.1126/science.7886451. [DOI] [PubMed] [Google Scholar]
  10. Harada Y., Akasaka K., Shimada H., Peterson K. J., Davidson E. H., Satoh N. Spatial expression of a forkhead homologue in the sea urchin embryo. Mech Dev. 1996 Dec;60(2):163–173. doi: 10.1016/s0925-4773(96)00608-9. [DOI] [PubMed] [Google Scholar]
  11. Holland P. W., Hacker A. M., Williams N. A. A molecular analysis of the phylogenetic affinities of Saccoglossus cambrensis Brambell & Cole (Hemichordata). Philos Trans R Soc Lond B Biol Sci. 1991 Jun 29;332(1264):185–189. doi: 10.1098/rstb.1991.0048. [DOI] [PubMed] [Google Scholar]
  12. Holland P. W., Holland L. Z., Williams N. A., Holland N. D. An amphioxus homeobox gene: sequence conservation, spatial expression during development and insights into vertebrate evolution. Development. 1992 Nov;116(3):653–661. doi: 10.1242/dev.116.3.653. [DOI] [PubMed] [Google Scholar]
  13. Holley S. A., Jackson P. D., Sasai Y., Lu B., De Robertis E. M., Hoffmann F. M., Ferguson E. L. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature. 1995 Jul 20;376(6537):249–253. doi: 10.1038/376249a0. [DOI] [PubMed] [Google Scholar]
  14. Kempf S. C., Page L. R., Pires A. Development of serotonin-like immunoreactivity in the embryos and larvae of nudibranch mollusks with emphasis on the structure and possible function of the apical sensory organ. J Comp Neurol. 1997 Sep 29;386(3):507–528. doi: 10.1002/(sici)1096-9861(19970929)386:3<507::aid-cne12>3.0.co;2-7. [DOI] [PubMed] [Google Scholar]
  15. Kispert A., Herrmann B. G., Leptin M., Reuter R. Homologs of the mouse Brachyury gene are involved in the specification of posterior terminal structures in Drosophila, Tribolium, and Locusta. Genes Dev. 1994 Sep 15;8(18):2137–2150. doi: 10.1101/gad.8.18.2137. [DOI] [PubMed] [Google Scholar]
  16. Mackey L. Y., Winnepenninckx B., De Wachter R., Backeljau T., Emschermann P., Garey J. R. 18S rRNA suggests that Entoprocta are protostomes, unrelated to Ectoprocta. J Mol Evol. 1996 May;42(5):552–559. doi: 10.1007/BF02352285. [DOI] [PubMed] [Google Scholar]
  17. Marois R., Croll R. P. Development of serotoninlike immunoreactivity in the embryonic nervous system of the snail Lymnaea stagnalis. J Comp Neurol. 1992 Aug 8;322(2):255–265. doi: 10.1002/cne.903220211. [DOI] [PubMed] [Google Scholar]
  18. McCauley D. W. Serotonin plays an early role in the metamorphosis of the hydrozoan Phialidium gregarium. Dev Biol. 1997 Oct 15;190(2):229–240. doi: 10.1006/dbio.1997.8698. [DOI] [PubMed] [Google Scholar]
  19. Murakami A. Control of ciliary beat frequency in the gill of Mytilus--I. Activation of the lateral cilia by cyclic AMP. Comp Biochem Physiol C. 1987;86(2):273–279. doi: 10.1016/0742-8413(87)90079-x. [DOI] [PubMed] [Google Scholar]
  20. Peterson K. J., Harada Y., Cameron R. A., Davidson E. H. Expression pattern of Brachyury and Not in the sea urchin: comparative implications for the origins of mesoderm in the basal deuterostomes. Dev Biol. 1999 Mar 15;207(2):419–431. doi: 10.1006/dbio.1998.9177. [DOI] [PubMed] [Google Scholar]
  21. Shubin N., Tabin C., Carroll S. Fossils, genes and the evolution of animal limbs. Nature. 1997 Aug 14;388(6643):639–648. doi: 10.1038/41710. [DOI] [PubMed] [Google Scholar]
  22. Wada H., Saiga H., Satoh N., Holland P. W. Tripartite organization of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax-2/5/8, Hox and Otx genes. Development. 1998 Mar;125(6):1113–1122. doi: 10.1242/dev.125.6.1113. [DOI] [PubMed] [Google Scholar]
  23. Wallace J. A. An immunocytochemical study of the development of central serotoninergic neurons in the chick embryo. J Comp Neurol. 1985 Jun 22;236(4):443–453. doi: 10.1002/cne.902360403. [DOI] [PubMed] [Google Scholar]
  24. Wallace J. A., Lauder J. M. Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res Bull. 1983 Apr;10(4):459–479. doi: 10.1016/0361-9230(83)90144-2. [DOI] [PubMed] [Google Scholar]
  25. Weigel D., Jürgens G., Küttner F., Seifert E., Jäckle H. The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell. 1989 May 19;57(4):645–658. doi: 10.1016/0092-8674(89)90133-5. [DOI] [PubMed] [Google Scholar]
  26. Williams N. A., Holland P. W. Molecular evolution of the brain of chordates. Brain Behav Evol. 1998;52(4-5):177–185. doi: 10.1159/000006562. [DOI] [PubMed] [Google Scholar]
  27. Yasuo H., Satoh N. Function of vertebrate T gene. Nature. 1993 Aug 12;364(6438):582–583. doi: 10.1038/364582b0. [DOI] [PubMed] [Google Scholar]
  28. de Rosa R., Grenier J. K., Andreeva T., Cook C. E., Adoutte A., Akam M., Carroll S. B., Balavoine G. Hox genes in brachiopods and priapulids and protostome evolution. Nature. 1999 Jun 24;399(6738):772–776. doi: 10.1038/21631. [DOI] [PubMed] [Google Scholar]
  29. van Mier P., Joosten H. W., van Rheden R., ten Donkelaar H. J. The development of serotonergic raphespinal projections in Xenopus laevis. Int J Dev Neurosci. 1986;4(5):465–475. doi: 10.1016/0736-5748(86)90028-6. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES