Skip to main content
SpringerLink
Log in

Immunofluorescence analysis of the internal brain anatomy of Nereis diversicolor (Polychaeta, Annelida)

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Comparative analyses of neuroanatomical characters can make valuable contributions to the inference of phylogenetic relationships. Whereas investigations in this field are numerous for arthropods, in-depth studies on other protostomes are sparse. Here, we provide a survey of the internal neuroarchitecture of the brain of the aciculate ragworm Nereis diversicolor (Polychaeta, Annelida). Descriptions are based on confocal laser scanning microscope analyses of brain sections labeled with the nuclear marker DAPI and antibodies raised against FMRF-amide, serotonin, and histamine. Autofluorescence of the nervous tissue has been utilized to further elucidate the anatomical structures of the brain. The architecture of two major brain compartments, i.e., the paired mushroom bodies and the central optic neuropil, is described in detail. The findings are compared with existent literature on polychaete neuroanatomy and on arthropod neuroanatomy, and possible phylogenetic implications are outlined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aguinaldo AM, Turbeville JM, Linford LS, Rivera MC, Garey JR, Raff RA, Lake JA (1997) Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387:489–493

    Article  PubMed  CAS  Google Scholar 

  • Baratte B, Gras-Masse H, Ricart G, Bulet P, Dhainaut-Courtois N (1991) Isolation and characterization of authentic Phe-Met-Arg-Phe-NH2 and the novel Phe-Thr-Arg-Phe-NH2 peptide from Nereis diversicolor. Eur J Biochem 198:627–633

    Article  PubMed  CAS  Google Scholar 

  • Dhainaut-Courtois N, Dubois M, Tramu G, Masson M (1985) Occurrence and coexistence in Nereis diversicolor O.F. Müller (Annelida Polychaeta) of substances immunologically related to vertebrate neuropeptides. Cell Tissue Res 242:97–108

    Article  PubMed  CAS  Google Scholar 

  • Dorsett DA, Hyde R (1969) The fine structure of the compound sense organs on the cirri of Nereis diversicolor. Z Zellforsch 97:512–527

    Article  PubMed  CAS  Google Scholar 

  • Engelhardt RP, Dhainaut-Courtois N, Tramu G (1982) Immunohistochemical demonstration of a CCK-like peptide in the nervous system of a marine annelid worm, Nereis diversicolor O.F. Müller. Cell Tissue Res 227:401–411

    Article  PubMed  CAS  Google Scholar 

  • Fanenbruck M, Harzsch S (2005) A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia, Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager, 1987 (Remipedia, Speleonectidae): implications for arthropod relationships. Arthropod Struct Dev 34:343–378

    Article  Google Scholar 

  • Halanych KM (2004) The new view of animal phylogeny. Annu Rev Ecol Evol Syst 35:229–256

    Article  Google Scholar 

  • Hanström B (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Springer, Berlin

    Google Scholar 

  • Harzsch S (2002) Neurobiologie und Evolutionsforschung: Neurophylogenie und die Stammesgeschichte der Euarthropoda. Neuroforum 4/02:267–273

    Google Scholar 

  • Holmgren N (1916) Zur vergleichenden Anatomie des Gehirns von Polychaeten etc. Kungl Sv Vet Akademiens Handlingar 56:1

    Google Scholar 

  • Loesel R (2005) The arthropod brain: retracing six hundred million years of evolution. Arthropod Struct Dev 34:207–209

    Article  Google Scholar 

  • Loesel R, Nässel DR, Strausfeld NJ (2002) Common design in a unique midline neuropil in the brains of arthropods. Arthropod Struct Dev 31:77–91

    Article  PubMed  Google Scholar 

  • Loesel R, Strausfeld NJ, Seyfarth EA, Agricola HJ (2005) A 450 million year Leitmotif for a locomotor control center in the brain: conserved neuroarchitecture of the central complex of chelicerates and hexapods. In: Zimmermann H, Krieglstein K (eds), Proc. 30th Göttingen Neurobiology Conference and 6th meeting German Neuroscience Society Neuroforum 2005, 1 Suppl (262A)

  • Mellon DF Jr, Alones V, Lawrence MD (1992) Anatomy and fine structure of neurons in the deutocerebral projection pathway of the crayfish olfactory system. J Comp Neurol 321:93–111

    Article  PubMed  Google Scholar 

  • Nielsen C (2001) Animal evolution: interrelationships of the living phyla. 2nd edn. Oxford University Press, Oxford

    Google Scholar 

  • Orrhage L, Müller M (2005) Morphology of the nervous system of Polychaeta (Annelida). Hydrobiologia 535/536:79–111

    Article  Google Scholar 

  • Porchet M, Dhainaut-Courtois N (1988) Neuropeptides and monoamines in annelids. In: Thorndyke MC, Goldsworthy GJ (eds) Neurohormones in invertebrates. Cambridge University Press, Cambridge, pp 219–234

    Google Scholar 

  • Rodriguez J, Deinhard F (1960) Preparation of a semipermanent mounting medium for fluorescent antibody studies. Virology 12:316–317

    Article  PubMed  CAS  Google Scholar 

  • Rössler W, Oland LA, Higgins MR, Hildebrand JG, Tolbert LP (1999) Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. J Neurosci 22:9865–9877

    Google Scholar 

  • Rouse GW, Fauchald K (1998) Recent views on the status, delineation and classification of the Annelida. Am Zool 38:953–964

    Google Scholar 

  • Rouse GW, Pleijel F (2003) Problems in polychaete systematics. Hydrobiologia 496:175–189

    Article  Google Scholar 

  • Scholtz G (2002) The Articulata hypothesis—or what is a segment? Organisms Diversity Evol 2:197–215

    Article  Google Scholar 

  • Scholtz G, Edgecombe GD (2005) Heads, Hox and the phylogenetic position of trilobites. Crustacea and arthropod relationships. Crustacean Issues 16:139–165

    Google Scholar 

  • Strausfeld NJ (1998) Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav Evol 52:186–206

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ (2005) The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Struct Dev 34:235–256

    Article  Google Scholar 

  • Strausfeld NJ, Weltzien P, Barth FG (1993) Two visual systems in one brain: neuropils serving the principal eyes of the spider Cupiennius salei. J Comp Neurol 328:63–75

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ, Buschbeck EK, Gomez RS (1995) The arthropod mushroom body: its functional roles, evolutionary enigmas and mistaken identities. In: Breidbach O, Kutsch W (eds) The nervous systems of invertebrates: an evolutionary and comparative approach. Birkhäuser, Basel, pp 349–381

    Google Scholar 

  • Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretation of arthropod mushroom bodies. Learn Mem 5:11–37

    PubMed  CAS  Google Scholar 

  • Strausfeld NJ, Strausfeld CM, Loesel R, Rowell D, Stowe S (2006a) Arthropod phylogeny: onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage. Proc R Soc Lond [Biol] 273:1857–1866

    Article  Google Scholar 

  • Strausfeld NJ, Strausfeld CM, Stowe S, Rowell D, Loesel R (2006b) The organization and evolutionary implications of neuropils and their neurons in the brain of the onychophoran Euperipatoides rowelli. Arthropod Struct Dev 35:169–196

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Prof. Thomas Bartolomaeus (FU Berlin, Germany) for providing us with an ample supply of N. diversicolor specimens and Dr. Harald Hausen (FU Berlin, Germany) for practical advice.

Author information

Authors and Affiliations

  1. Department of Developmental Biology and Morphology of Animals, Institute for Biology II, RWTH Aachen, 52056, Aachen, Germany

    C. M. Heuer & R. Loesel

Authors
  1. C. M. Heuer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Loesel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Loesel.

Additional information

Funding for this study was provided by DFG grant LO797/3-1 as part of the Priority Program 1174—“Deep Metazoan Phylogeny” of the Deutsche Forschungsgemeinschaft.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heuer, C.M., Loesel, R. Immunofluorescence analysis of the internal brain anatomy of Nereis diversicolor (Polychaeta, Annelida). Cell Tissue Res 331, 713–724 (2008). https://doi.org/10.1007/s00441-007-0535-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-007-0535-y

Keywords

Search

Navigation