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Development of the nervous system in the "head" of Limulus polyphemus (Chelicerata: Xiphosura): morphological evidence for a correspondence between the segments of the chelicerae and of the (first) antennae of Mandibulata

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Abstract

We investigated brain development in the horseshoe crab Limulus polyphemus and several other arthropods via immunocytochemical methods, i.e. antibody stainings against acetylated α-tubulin and synapsin. According to the traditional view, the first appendage-bearing segment in chelicerates (the chelicerae) is not homologous to the first appendage-bearing segment of mandibulates (first antenna, deutocerebrum) but to the segment of the second antenna (tritocerebrum) or the intercalary segment in hexapods and myriapods. Accordingly, the segment of the deutocerebrum in chelicerates would be completely reduced. The main arguments for this view are: (1) the postoral origin of the cheliceral ganglion, (2) a poststomodaeal commissure, and (3) a connection of the cheliceral ganglion to the stomatogastric system. Our data show that these arguments are not convincing. During the development of horseshoe crabs there is no evidence for a former additional segment in front of the chelicerae. Instead, comparison of the brain structure (neuropil ring) between chelicerates, crustaceans and insects shows remarkable similarities. Furthermore, the cheliceral commissure in horseshoe crabs runs mainly praestomodaeal, which would be unique for a tritocerebral commissure. An unbiased view of the developing nervous system in the "head" of chelicerates, crustaceans and insects leads to a homologisation of the cheliceral segment and that of the (first) antenna (= deutocerebrum) of mandibulates that is also congruous to the interpretation of the Hox gene expression patterns. Thus, our data provide morphological evidence for the existence of a chelicerate deutocerebrum.

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References

  • Abzhanov A, Popadic A, Kaufman TC (1999) Chelicerate Hox genes and the homology of arthropod segments. Evol Dev 1(2):77–89

    Article  CAS  PubMed  Google Scholar 

  • Babu KS (1965) Anatomy of the central nervous system of arachnids. Zool Jb Anat 82:1–154

    Google Scholar 

  • Böhm H, Dybek E, Heinzel H-G (2001) Anatomy and in vivo activity of neurons connecting the crustacean stomatogastric nervous system to the brain. J Comp Physiol A 187:393–403

    Article  PubMed  Google Scholar 

  • Boyan G, Williams L (2002) Building the antennal lobe: engrailed expression reveals a contribution from protocerebral neuroblasts in the grasshopper Schistocerca gregaria. Arthropod Struct Dev 29(3):267–274

    Article  Google Scholar 

  • Brauer A (1894) Beiträge zur Entwicklungsgeschichte des Skorpions I. Z Wiss Zool 57:402–432

    Google Scholar 

  • Brauer A (1895) Beiträge zur Entwicklungsgeschichte des Skorpions II. Z Wiss Zool 59:351–435

    Google Scholar 

  • Budd GE (2002) A palaeontological solution to the arthropod head problem. Nature 417:271–275

    Article  CAS  PubMed  Google Scholar 

  • Campos-Ortega JA, Hartenstein V (1997) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New York

  • Cook CE, Smith LM, Telford MJ, Bastinello A, Akam A (2001) Hox genes and the phylogeny of the arthropods. Curr Biol 11:759–763

    Article  CAS  PubMed  Google Scholar 

  • Damen WGM (2002) Parasegmental organization of the spider embryo implies that the parasegment is an evolutionary conserved entity in arthropod embryogenesis. Development 129:1239–1250

    CAS  PubMed  Google Scholar 

  • Damen WGM, Hausdorf M, Seyfarth E-A, Tautz D (1998) A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci USA 95:10665–10670

    CAS  PubMed  Google Scholar 

  • Dohle W (1997) Are the insects more closely related to the crustaceans than to the myriapods? Entomol Scand Suppl 51:7–16

    Google Scholar 

  • Dohle W (2001) Are the insects terrestrial crustaceans? Ann Soc Entomol Fr 3(1–2):85–103

    Google Scholar 

  • Dumont JPC, Wine JJ (1987) The telson flexor muscular system of the crayfish. I. Homology with the fast flexor system. J Exp Biol 127:249–277

    Google Scholar 

  • Garzino V, Reichert H (1994) Early embryonic expression of a 60-kDa glycoprotein in the developing nervous system of the lobster. J Comp Neurol 346:572–582

    CAS  PubMed  Google Scholar 

  • Giribet G, Edgecombe GD, Wheeler WC (2001) Arthropod phylogeny based on eight molecular loci and morphology. Nature 413:157–161

    Article  CAS  PubMed  Google Scholar 

  • Goodrich ES (1897) On the relation of the arthropod head to the annelid prostomium. Q J Microsc Sci 40:147–268

    Google Scholar 

  • Gruner H-E (ed) (1993) Lehrbuch der Speziellen Zoologie, Bd.1 Wirbellose Tiere, 4. Teil Arthropoda. (Begr. A. Kästner) Fischer, Jena

  • Hanström B. (1928) Das Nervensystem der wirbellosen Tiere. Springer, Berlin Heidelberg New York

  • Harzsch S (1997) Immunocytochemical detection of acetylated α-tubulin and Drosophila synapsin in the embryonic nervous system. Int J Dev Biol 41:477–484

    Google Scholar 

  • Harzsch S, Glötzner J (2002) An immunohistochemical study of structure and development of the nervous system in the brine shrimp Artemia salina Linnaeus, 1758 (Branchiopoda, Anostraca) with remarks on the evolution of the arthropod brain. Arthropod Struct Dev 30:251–270

    Article  Google Scholar 

  • Henry LM (1950) The cephalic nervous system of Limulus polyphemus Linnaeus (Arthropoda: Xiphosura). Microentomology 15(4):129–139

    Google Scholar 

  • Holmgren N (1916) Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. Vet Ak Handl (Stockholm) 56:1–303

    Google Scholar 

  • Hughes CL, Kaufman TC (2002) Exploring the myriapod bodyplan: expression patterns of the ten Hox genes in a centipede. Development 129:1225–1238

    CAS  PubMed  Google Scholar 

  • Hwang UW, Friedrich M, Tautz D, Park CJ, Kim W (2001) Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413:154–157

    Article  CAS  PubMed  Google Scholar 

  • Ivanoff PP (1933) Die embryonale Entwicklung von Limulus moluccanus. Zool Jahrb Anat (56):164–348

    Google Scholar 

  • Johansson G (1933) Beiträge zur Kenntnis der Morphologie und Entwicklung des Gehirns von Limulus polyphemus. Acta Zool 14:1–100

    Google Scholar 

  • Kingsley JS (1892) The embryology of Limulus. J Morphol 7:35–68

    Google Scholar 

  • Kishinouye K (1891) On the development of Limulus longispina. J Coll Sci Univ Jpn 5:53–100

    Google Scholar 

  • Lauterbach K-E (1980) Schlüsselereignisse in der Evolution des Grundplans der Mandibulata (Arthropoda). Abh Verh Naturwiss Ver Hamburg 20:105–161

    Google Scholar 

  • Pappenheim P (1903) Beitrag zur Kenntnis der Entwicklungsgeschichte von Dolmedes fibriatus Clerk, mit besonderer Berücksichtigung der Bildung des Gehirns und der Augen. Z Wiss Zool 74:109–154

    Google Scholar 

  • Patten W, Redenbaugh WA (1899) Studies on Limulus II. The nervous system of Limulus polyphemus, with observations upon the general anatomy. J Morphol 16:91–200

    Google Scholar 

  • Pross A (1966) Untersuchungen zur Entwicklungsgeschichte der Araneae (Pardosa hortensis (Thorell)) unter besonderer Berücksichtigung des vorderen Prosomaabschnittes. Z Morphol Oekol Tiere 58:38–108

    Google Scholar 

  • Pross A (1977) Diskussionsbeitrag zur Segmentierung des Cheliceraten-Kopfes. Zoomorphologie 86:183–196

    Google Scholar 

  • Rempel JG (1975) The evolution of the insect head: the endless dispute. Quaest Entomol 11:7–25

    Google Scholar 

  • Richter S (2002) The Tetraconata concept: hexapod-crustacean relationships and the phylogeny of Crustacea. Org Diversity Evol 2: 217–238

    Google Scholar 

  • Richter S, Edgecombe GD, Wilson GDF (2002) The lacinia mobilis and similar structures – a valuable character in arthropod phylogenetics? Zool Anz 241 (in press)

  • Rogers BT, Kaufman TC (1998) Structure of the Insect head in ontogeny and phylogeny: a view from Drosophila. Int Rev Cytol 174:1–84

    Google Scholar 

  • Sandeman D, Sandeman R, Derby C, Schmidt M (1992) Morphology of the brain of crayfish, crabs, and spiny lobsters: a common nomenclature for homologous structures. Biol Bull 183:304–326

    Google Scholar 

  • Scholl G (1977) Beiträge zur Embryonalentwicklung von Limulus polyphemus L. (Chelicerata, Xiphosura). Zoomorphologie 86:99–154

    Google Scholar 

  • Scholtz G (1990) The formation, differentiation and segmentation of the post-naupliar germ band of the amphipod Gammarus pulex L. (Crustacea, Malacostraca, Peradarida). Proc R Soc Lond B 239:163–211

    Google Scholar 

  • Scholtz G (1997) Cleavage, germ band formation and head segmentation: the ground pattern of Euarthropoda. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman & Hall, London, pp 317–332

  • Scholtz G (2001) Evolution of developmental patterns in arthropods the analysis of gene expression and its bearing on morphology and phylogenetics. Zoology 103:99–111

    CAS  Google Scholar 

  • Scholtz G, Mittmann B, Gerberding M (1998) The pattern of Distal-less expression in the mouthparts of crustaceans, myriapods and insects: new evidence for a gnathobasic mandible and the common origin of Mandibulata. Int J Dev Biol 42:801–810

    CAS  PubMed  Google Scholar 

  • Siewing R (1963) Zum Problem der Arthropodenkopfsegmentierung. Zool Anz 170:429–468

    Google Scholar 

  • Snodgrass RE (1960) Facts and theories concerning the insect head. Smithson Misc Collect 142(1):1–61

    Google Scholar 

  • Telford M, Thomas RH (1998) Expression of homeobox genes shows chelicerate arthropods retain their deutocerebral segment. Proc Natl Acad Sci USA 95:10671–10675

    Article  CAS  PubMed  Google Scholar 

  • Viallanes MH (1893) Etudes histologiques et organologiques sur les centres nerveux et les organs de sens des animaux articulés. Ann Sci Nat Serv VII Zool 14:405–456

    Google Scholar 

  • Walossek D (1993) The upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea. Foss Strata 32:3–202

    Google Scholar 

  • Weygoldt P (1985) Ontogeny in the arachnid central nervous system. In: Barth FG (ed) Neurobiology of Arachnids. Springer, Berlin Heidelberg New York, pp 20–37

  • Winter G (1980) Beiträge zur Morphologie und Embryologie des vorderen Körperabschnitts (Cephalosoma) der Pantopoda Gerstaecker, 1863. Z Zool Syst Evol 18:27–61

    Google Scholar 

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Acknowledgements

We thank Robert B. Barlow (Woods Hole, Syracuse) for his extensive support while collecting eggs of Limulus polyphemus in Woods Hole. The scientific work in Woods Hole was partly supported by the National Science Foundation (USA) and the National Institute of Health (USA; both grants to Robert B. Barlow). Andreas Mölich (Institut für Tierphysiolgie, Humboldt-Universität) and Ekkehard Richter (Institut für Membranphysiologie) were very patient during confocal microscopy. The synorf1 antibody was a generous gift of Erich Buchner (Institut für Genetik, Würzburg). First eggs of Triops cancriformis were kindly provided by Erich Eder (Institut für Zoologie, Universität Wien). Preparation of Penaeus monodon was done by Frederike Alwes. Furthermore, we thank Richard H. Thomas (London) and Gregory Edgecombe (Sydney) for helpful comments and for linguistic assistance. This work was supported by the Deutsche Forschungsgemeinschaft (Scho442/7–1, Scho442/7–2).

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  1. Institut für Biologie, Vergleichende Zoologie, Humboldt-Universität zu Berlin, Philippstr. 13, 10115, Berlin, Germany

    Beate Mittmann & Gerhard Scholtz

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  1. Beate Mittmann
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  2. Gerhard Scholtz
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Correspondence to Beate Mittmann.

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Mittmann, B., Scholtz, G. Development of the nervous system in the "head" of Limulus polyphemus (Chelicerata: Xiphosura): morphological evidence for a correspondence between the segments of the chelicerae and of the (first) antennae of Mandibulata. Dev Genes Evol 213, 9–17 (2003). https://doi.org/10.1007/s00427-002-0285-5

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