Acta Biologica Hungarica

, Volume 55, Issue 1–4, pp 39–51 | Cite as

Comparative Morphology of Central Neuropils in the Brain of Arthropods and Its Evolutionary and Functional Implications

  • R. LoeselEmail author


Most insects and decapod crustaceans possess an assemblage of midline neuropils, the central complex. Recent phylogenetic studies show a sister-group relationship between hexapods and decapods, suggesting that central complexes in both groups are homologous structures derived from a basal ancestral neuropil [22]. This ancestral archetype of the central complex (lacking the protocerebral bridge) might be represented in the chilopods. Until recently, diplopods were regarded as closely related to chilopods and united within the taxon Myriapoda. The entire lack of a midline neuropil in diplopods, however, renders the monophyletic origin of the class Myriapoda unlikely [15]. In this study we used a palette of immunocytochemical and neuroanatomical methods to investigate mid-line neuropils in hitherto poorly examined arthropod groups. Of special interest for resolving arthropod phylogeny are onychophorans, who are believed to be an evolutionary ancient group that resembles the ancestors of modern arthropods. Striking similarities in central brain neuroarchitecture of the onychophoran Euperipatoides rowellii and of a chelicerate species, however, suggest a close phylogenetic relationship between these two groups. Our findings imply that onychophorans either represent the oldest form of the chelicerates or that extant onychophorans have developed from chelicerate-like ancestors by neoteny.


Central complex immunocytochemistry neuroanatomy Onychophora locomotor control 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Bausenwein, B., M ller, N. R., Heisenberg, M. (1994) Behavior-dependent activity labeling in the central complex of Drosophila during controlled visual stimulation. J. Comp. Neurol. 340, 255–268.CrossRefGoogle Scholar
  2. 2.
    Bodian, D. (1936) Anew method for staining nerve fibers and nerve endings in mounted paraffin sections. Anat. Rec. 65, 89–97.CrossRefGoogle Scholar
  3. 3.
    Bordeaux, H. B. (1979) Arthropod Phylogeny with Special Reference to Insects. Wiley, New York.Google Scholar
  4. 4.
    Brusca, R. C., Brusca, G. J. (1990) Invertebrates. Sinauer, Sunderland.Google Scholar
  5. 5.
    Damen, W. G. M. (2002) Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 129, 1239–1250.PubMedGoogle Scholar
  6. 6.
    Dearden, P. K., Donly, C., Grbic, M. (2002) Expression of pair-rule gene homologues in a chelicerate: early patterning of the two-spotted spider mite Tetranychus urticae. Development 129, 5461–5472.CrossRefGoogle Scholar
  7. 7.
    Farley, R. D. (2001) Development of segments and appendages in embryos of the desert scorpion Paruroctomus mesaensis (Scorpiones: Vaejovidae). J. Morphol. 250, 70–88.CrossRefGoogle Scholar
  8. 8.
    Fl gel, J. H. L. (1878) ber den einheitlichen Bau des Gehirns in den verschiedenen Insektenordnungen. Z. Wiss. Zool. 30 (supplement), 556–592.Google Scholar
  9. 9.
    Grenier, J. K., Garber, T. L., Warren, R., Whitington, P. M., Carroll, S. (1997) Evolution of the entire arthropod Hox gene set predated the origin and radiation of the onychophoran/arthropod clade. Curr. Biol. 7, 547–553.CrossRefGoogle Scholar
  10. 10.
    Hanesch, U., Fischbach, K. F., Heisenberg, M. (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res. 257, 343–366.CrossRefGoogle Scholar
  11. 11.
    Holmgren, N. (1916) Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. K. Svenska Vetensk. Akad. Handl. 56, 1–303.Google Scholar
  12. 12.
    Homberg, U. (1985) Interneurons in the central complex in the bee brain (Apis mellifera, L.). J. Insect Physiol. 31, 251–264.CrossRefGoogle Scholar
  13. 13.
    Homberg, U. (1991) Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J. Comp. Neurol. 303, 245–254.CrossRefGoogle Scholar
  14. 14.
    Ioffe, I. D. (1963) Structure of the brain of Dermacentor pictus Herm. (Chelicerata, Acarina). Zool. Zh. 42, 1472–1484.Google Scholar
  15. 15.
    Loesel, R., N ssel, D. R., Strausfeld, N. J. (2002) Common design in a unique midline neuropil in the brains of arthropods. Arthropod Structure & Development 31, 77–91.CrossRefGoogle Scholar
  16. 16.
    Milde, J. J. (1988) Visual responses of interneurons in the posterior median protocerebrum and the central complex of the honeybee Apis mellifera. J. Insect Physiol. 34, 427–436.CrossRefGoogle Scholar
  17. 17.
    Popadic, A., Panganiban, G., Rusch, D., Shear, W. A., Kaufman, T. C. (1998) Molecular evidence for the gnathobasic derivation of arthropod mandibles and for the appendicular origin of the labrum and other structures. Dev. Genes. Evol. 208, 142–150.CrossRefGoogle Scholar
  18. 18.
    Renn, S. C., Armstrong, J. D., Yang, M., Wang, Z., An, K., Kaiser, K., Taghert, P. H. (1999) Genetic analysis of the Drosophila ellipsoid body neuropil: Organization and development of the central complex. J. Neurobiol. 41, 189–207.CrossRefGoogle Scholar
  19. 19.
    Sandeman, D., Scholz, G. (1995) Ground plans, evolutionary changes and homologies in decapod crustacean brains. In: Breidbach, O., Kutsch, W. (eds) The Nervous System of Invertebrates: An Evolutionary and Comparative Approach. Birkh user, Basel, pp. 329–347.CrossRefGoogle Scholar
  20. 20.
    Stay, B., Chan, K. K., Woodhead, A. P. (1992) Allatostatin-immunoreactive neurons projecting to the corpora allata of adult Diploptera punctata. Cell Tissue Res. 270, 15–23.CrossRefGoogle Scholar
  21. 21.
    Strausfeld, N. J. (1976) Atlas of an insect brain. Springer, Heidelberg.CrossRefGoogle Scholar
  22. 22.
    Strausfeld, N. J. (1998) Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav. Evol. 52, 186–206.CrossRefGoogle Scholar
  23. 23.
    Strausfeld, N. J. (1999) A brain region in insects that supervises walking. Progr. Brain Res. 123, 273 284.Google Scholar
  24. 24.
    Strausfeld, N. J., Barth, F. G. (1993) Two visual systems in one brain: Neuropils serving the secondary eyes of the spider Cupiennius salei. J. Comp. Neurol. 328, 43–62.CrossRefGoogle Scholar
  25. 25.
    Strausfeld, N. J., Weltzien, P., Barth, F. G. (1993) Two visual systems in one brain: Neuropils serving the principal eyes of the spider Cupiennius salei. J. Comp. Neurol. 328, 63–75.CrossRefGoogle Scholar
  26. 26.
    Strauss, R., Heisenberg, M. (1990) Coordination of legs during straight walking and turning in Drosophila melanogaster. J. Comp. Physiol. A 167, 403–412.CrossRefGoogle Scholar
  27. 27.
    Strauss, R., Trinath, T. (1996) Is walking in a straight line controlled by the central complex? Evidence from a new Drosophila mutant. In: Elsner, N., Schnitzler, U. (eds), Proceedings of the 24th G ttingen Neurobiology Conference. Vol II. Thieme, Stuttgart, p. 135.Google Scholar
  28. 28.
    Strauss, R., Hanesch, U., Kinkelin, M., Wolf, R., Heisenberg, M. (1992) No-bridge of Drosophila melanogaster portrait of a structural mutant of the central complex. J. Neurogen. 8, 125–155.CrossRefGoogle Scholar
  29. 29.
    Utting, M., Agricola, H. J., Sandeman, R., Sandeman, D. (2000) Central complex in the brain of crayfish and its possible homology with that of insects. J. Comp. Neurol. 416, 245–261.CrossRefGoogle Scholar
  30. 30.
    Vitzthum, H., Mueller, M., Homberg, U. (2002) Neurons of the central complex of the locust Schistocerca gregaria are sensitive to polarized light. J. Neurosci. 22, 1114–1125.CrossRefGoogle Scholar
  31. 31.
    Wedeen, C. J., Kostriken, R. G., Leach, D., Whitington, P. (1997) Segmentally iterated expression of an engrailed-class gene in the embryo of an Australian onychophoran. Dev. Genes Evol. 270, 282–286.CrossRefGoogle Scholar
  32. 32.
    Weltzien, P., Barth, F. G. (1991) Volumetric measurements do not demonstrate that the spider brain central body has a special role in web building. J. Morphol. 207, 1–8.CrossRefGoogle Scholar
  33. 33.
    Williams, J. L. D. (1975) Anatomical studies of the insect central nervous system: A ground-plan of the midbrain and an introduction to the central complex in the locust Schistocerca gregaria (Orthoptera). J. Zool. 176, 67–86.Google Scholar
  34. 34.
    Winther, Å. M. E., N ssel, D. R. (2001) Intestinal peptides as circulating hormones: release of tachykinin-related peptide from the midgut of locust and cockroach. J. Exp. Biol. 204, 1269–1280.PubMedGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2004

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Department of Developmental Biology and Morphology of AnimalsInstitute of Biology II, RWTH AachenGermany

Personalised recommendations