Advertisement

Development Genes and Evolution

, Volume 217, Issue 11–12, pp 791–799 | Cite as

The Engrailed-expressing secondary head spots in the embryonic crayfish brain: examples for a group of homologous neurons in Crustacea and Hexapoda?

  • Silvia Sintoni
  • Kathia Fabritius-Vilpoux
  • Steffen Harzsch
Short Communication

Abstract

Hexapoda have been traditionally seen as the closest relatives of the Myriapoda (Tracheata hypothesis) but molecular studies have challenged this hypothesis and rather have suggested a close relationship of hexapods and crustaceans (Tetraconata hypothesis). In this new debate, data on the structure and development of the arthropod nervous system contribute important new data (“neurophylogeny”). Neurophylogenetic studies have already provided several examples for individually identifiably neurons in the ventral nerve cord that are homologous between insects and crustaceans. In the present report, we have analysed the emergence of Engrailed-expressing cells in the embryonic brain of a parthenogenetic crayfish, the marbled crayfish (Marmorkrebs), and have compared our findings to the pattern previously reported from insects. Our data suggest that a group of six Engrailed-expressing neurons in the optic anlagen, the so-called secondary head spot cells can be homologised between crayfish and the grasshopper. In the grasshopper, these cells are supposed to be involved in establishing the primary axon scaffold of the brain. Our data provide the first example for a cluster of brain neurons that can be homologised between insects and crustaceans and show that even at the level of certain cell groups, brain structures are evolutionary conserved in these two groups.

Keywords

Arthropod Neurophylogeny Evolution Engrailed Tetraconata 

Notes

Acknowledgements

We gratefully acknowledge the comments of one of the anonymous reviewers that greatly improved the manuscript. The 4D9 anti-En/invected monoclonal antibody developed by Corey Goodman (University of California, Berkeley, Department of Molecular and Cell Biology, 519 Life Sciences Addition, Berkeley, CA 94720, USA) was obtained from the Developmental Studies Hybridoma Bank developed under the auspices of the NICHD and maintained by The University of Iowa, Department of Biological Sciences, Iowa City, IA 52242, USA. S.S. is the recipient of an EC fellowship within the MOLMORPH network under the 6th Framework Programme Marie Curie Host Fellowships for Early Stage Research Training (EST; contract number MEST-CT-2005-020542). The experimental part of this study was supported by DFG grant HA 2540/6 and a Heisenberg fellowship of the DFG to S.H.

Supplementary material

427_2007_189_Fig1_ESM.jpg (97 kb)
Supplementary figure

Confocal laser-scan images of a tertiary head cell at E50%; gallery of a seven-image stack (0,44 μm interval) covering a total z-distance of 2,64μm (JPEG 99 kb)

References

  1. Abzhanov A, Kaufman TC (2000) Evolution of distinct expression patterns for engrailed paralogues in higher crustaceans (Malacostraca). Dev Genes Evol 210:493–506CrossRefGoogle Scholar
  2. Alwes F, Scholtz G (2006) Stages and other aspects of the embryology of the parthenogenetic Marmorkrebs (Decapoda, Reptantia, Astacida). Dev Genes Evol 216:169–184PubMedCrossRefGoogle Scholar
  3. Boyan GS, Williams JLD (2002) A single cell analysis of engrailed expression in the early embryonic brain of the grasshopper Schistocerca gregaria: ontogeny and identity of the secondary head spots. Arthropod Struct Dev 3:207–218CrossRefGoogle Scholar
  4. Boyan G, Reichert H, Hirth F (2003) Commissure formation in the embryonic insect brain. Arthropod Struct Dev 32:61–78CrossRefGoogle Scholar
  5. Brown SJ, Patel NH, Denell RE (1994) Embryonic expression of the single Tribolium engrailed homolog. Dev Genet 15:7–18PubMedCrossRefGoogle Scholar
  6. Duman-Scheel M, Patel N (1999) Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 126:2327–2334PubMedGoogle Scholar
  7. Harzsch S (2003a) Ontogeny of the ventral nerve cord in malacostracan crustaceans: a common plan for neuronal development in Crustacea, Hexapoda and other Arthropoda? Arthropod Struct Dev 32:17–37CrossRefGoogle Scholar
  8. Harzsch S (2003b) Evolution of identified arthropod neurons: the serotonergic system in relation to engrailed-expressing cells in the embryonic ventral nerve cord of the American lobster Homarus americanus Milne Edwards, 1873 (Malacostraca, Pleocyemata, Homarida). Dev Biol 258(1):44–56PubMedCrossRefGoogle Scholar
  9. Harzsch S (2006) Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phylogeny. Integr Comp Biol 46:162–194CrossRefGoogle Scholar
  10. Harzsch S, Müller CH, Wolf H (2005) From variable to constant cell numbers: cellular characteristics of the arthropod nervous system argue against a sister-group relationship of Chelicerata and “Myriapoda” but favour the Mandibulata concept. Dev Genes Evol 215:53–68PubMedCrossRefGoogle Scholar
  11. Joly W, Mugat B, Maschat F (2007) Engrailed controls the organization of the ventral nerve cord through frazzled regulation. Dev Biol 301:542–554PubMedCrossRefGoogle Scholar
  12. Martin P, Kohlmann K, Scholtz G (2007) The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring. Naturwissenschaften 94:843–846PubMedCrossRefGoogle Scholar
  13. Patel NH (1994) Evolution of arthropod segmentation: insights from comparisons of gene expression patterns. Development 120S:201–207Google Scholar
  14. Patel NH, Kornberg TB, Goodman CS (1989) Expression of engrailed during segmentation in grasshopper and crayfish. Development 107:201–212PubMedGoogle Scholar
  15. Rieger V, Harzsch S (2007) Embryonic development of the histaminergic system in the ventral nerve cord of the marbled Crayfish (Marmorkrebs). Tissue Cell (in press)Google Scholar
  16. Rogers BT, Kaufman TC (1996) Structure of the insect head as revealed by the En protein pattern in developing embryos. Development 122:3419–3432PubMedGoogle Scholar
  17. Schmidt-Ott U, Technau GM (1992) Expression of en and wg in the embryonic head and brain of Drosophila indicates a refolded band of seven segment remnants. Development 116:111–125PubMedGoogle Scholar
  18. Schmidt-Ott U, Sander K, Technau GM (1994) Expression of engrailed in embryos of a beetle and five dipteran species with special reference to the terminal regions. Roux’s Arch Dev Biol 203:298–303CrossRefGoogle Scholar
  19. Scholtz G (1995) Head segmentation in Crustacea—an immunocytochemical study. Zoology 98:104–114Google Scholar
  20. Scholtz G (2001) Evolution of developmental patterns in arthropods—the contribution of gene expression to morphology and phylogenetics. Zoology 103:99–111Google Scholar
  21. Scholtz G, Dohle W, Sandeman RE, Richter S (1993) Expression of engrailed can be lost and regained in cells of one clone in crustacean embryos. Int J Dev Biol 37:299–304PubMedGoogle Scholar
  22. Scholtz G, Patel NH, Dohle W (1994) Serially homologous engrailed stripes are generated via different cell lineages in the germ band of amphipod crustaceans (Malacostraca, Peracarida). Int J Dev Biol 38:471–478PubMedGoogle Scholar
  23. Scholtz G, Braband A, Tolley L, Reimann A, Mittmann B, Lukhaup C, Steuerwald F, Vogt G (2003) Ecology: parthenogenesis in an outsider crayfish. Nature 421:806PubMedCrossRefGoogle Scholar
  24. Seitz R, Vilpoux K, Hopp U, Harzsch S, Maier G (2005) Ontogeny of the Marmorkrebs (marbled crayfish): a parthenogenetic crayfish with unknown origin and phylogenetic position. J Exp Zool 303:393–405CrossRefGoogle Scholar
  25. Urbach R, Technau GM (2003) Early steps in building the insect brain: neuroblast formation and segmental patterning in the developing brain of different insect species. Arthropod Struct Dev 32:103–124CrossRefGoogle Scholar
  26. Urbach R, Technau GM, Breidbach O (2003) Spatial and temporal pattern of neuroblasts, proliferation, and engrailed expression during early brain development in Tenebrio molitor L. (Coleoptera). Arthropod Struct Dev 32:125–140CrossRefGoogle Scholar
  27. Vilpoux K, Sandeman R, Harzsch S (2006) Early embryonic development of the central nervous system in the Australian crayfish and the marbled crayfish (Marmorkrebs). Dev Genes Evol 216:209–223PubMedCrossRefGoogle Scholar
  28. Zacharias D, Williams JLD, Meier T, Reichert H (1993) Neurogenesis in the insect brain: cellular identification and molecular characterization of brain neuroblasts in the grasshopper embryo. Development 118:941–955Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Silvia Sintoni
    • 1
    • 2
  • Kathia Fabritius-Vilpoux
    • 1
  • Steffen Harzsch
    • 2
  1. 1.Fakultät für Naturwissenschaften, Institut für Neurobiologie and Sektion Biosystematische DokumentationUniversität UlmUlmGermany
  2. 2.Department of Evolutionary NeuroethologyMax Planck Institute for Chemical EcologyJenaGermany

Personalised recommendations