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Developmental mechanisms, homology and evolution of the insect peripheral nervous system

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Book cover The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach

Part of the book series: Experientia Supplementum ((EXS,volume 72))

Summary

Segmentally homologous neurogenesis and neuronal differentiation processes characterize the formation of the insect peripheral nervous system. These processes have been analyzed at the level of identified neurons and nerve branches in the grasshopper. During early embryogenesis a simple peripheral nerve scaffolding is established in each body segment. This scaffolding consists of serially reiterated segmental nerves, which are pioneered by afferent neurons situated in limb bud homologs, and of serially reiterated intersegmental nerves, which are pioneered by homologous body wall afferents. Subsequently, identified sets of serially homologous sensory neurons differentiate in a stereotyped spatiotemporal pattern in each segment and project their axons onto these nerves. Data on serial homology in the development of the peripheral nervous system, which were obtained on the basis of comparative structural and developmental data in the grasshopper, are supported by a large body of developmental and genetic data obtained using Drosophila wild-type and mutants. Indeed, a comparison of the results obtained in the grasshopper with those obtained from Drosophila shows that virtually the same pattern of peripheral nerves and major sensory structures is formed in both species. These findings indicate that the construction of the peripheral nervous system in extremely divergent modern insects relies on conserved developmental mechanisms that evolved in ancestral insects over 300 million years ago.

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References

  • Akam, M., Dawson, I. and Tear, G. (1988) Homeotic genes and the control of segment diversity. Development 104 (Suppl.): 123–133.

    Google Scholar 

  • Arbas, E.A. (1983) Neural correlates of flight loss in a mexican grasshopper, Barytettix psolus. I. Motor and sensory cells. J. Comp. Neurol. 216: 369–380.

    Article  PubMed  CAS  Google Scholar 

  • Arbas, E.A., Meinertzhagen, I.A. and Shaw, S.R. (1991) Evolution in nervous systems. Annu. Rev. Neurosci. 14: 9–38.

    Article  PubMed  CAS  Google Scholar 

  • Bastiani, M.J., DuLac, S.L. and Goodman, C.S. (1986) Guidance of neuronal growth cones in the grasshopper embryo. I. Recognition of specific axonal pathway by the pCC neuron. J. Neurosci. 6: 3518–3531.

    PubMed  CAS  Google Scholar 

  • Bate, C.M. (1978) Development of sensory systems in Arthropods. In: M. Jacobson (ed.): Handbook of Sensory Physiology. Springer Verlag, Berlin, Heidelberg, New York, pp. 1–53.

    Google Scholar 

  • Bentley, D., Keshishian, H., Shankland, M. and Toroian-Raymond A. (1979) Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. J. Embryol. Exp. Morph. 54: 47–74.

    CAS  Google Scholar 

  • Bentley, D. and Keshishian, H. (1982) Pathfinding by peripheral pioneer neurons in grasshoppers. Science 218: 1082–1088.

    Article  PubMed  CAS  Google Scholar 

  • Bickmeyer, U., Kalmring, K., Halex, H. and Mücke, A. (1992) The bimodal auditory-vibratory system of thoracic ventral nerve cord in Locusta migratoria. J. Exp. Zool. 264: 381–394.

    Article  CAS  Google Scholar 

  • Bier, E., Jan, L.Y. and Jan, Y.N. (1990) rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev. 4: 190–203.

    Article  PubMed  CAS  Google Scholar 

  • Blochlinger, K., Bodmer, R., Jack, J., Jan, L.Y. and Jan, Y.N. (1988) Primary structure and expression of a product from cut, a locus involved in specifying sensory organ identity in Drosophila. Nature 333: 629–635.

    CAS  Google Scholar 

  • Blochlinger, K., Jan, L.Y. and Jan, Y.N. (1993) Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila. Development 117: 441–450.

    CAS  Google Scholar 

  • Bodmer, R. and Jan, Y.N. (1987) Morphological differentiation of the embryonic peripheral neurons in Drosophila. Roux’s Arch. Dev. Biol. 196: 69–77.

    Article  Google Scholar 

  • Boyan, G. (1992) Common synaptic drive to segmentally homologous interneurons in the locust. J. Comp. Neurol. 321: 544–554.

    Article  PubMed  CAS  Google Scholar 

  • Boyan, G. (1993) Another look at insect audition: the tympanic receptors as an evolutionary specialization of the chordotonal organ. J. Insect Physiol. 39: 187–200.

    Article  Google Scholar 

  • Boyan, G. and Ball, E.E. (1993) The grasshopper, the fruitfly, and neuronal homology: answers to some fundamental questions in neurobiology. Progress in Neurobiol; in press.

    Google Scholar 

  • Campos-Ortega, J.A. and Hartenstein, B. (1985) The embryonic development of Drosophila melanogaster. Springer Verlag, Berlin.

    Google Scholar 

  • Caudy, M., and Bentley, D. (1986) Pioneer growth cone morphologies reveal proximal increase in substrate affinity within leg segments of grasshopper embryos. J. Neurosci. 6: 364–379.

    PubMed  CAS  Google Scholar 

  • Chu-LaGraff, Q., Wright, D.M., McNeil, L.K. and Doe, C.Q. (1991) The prospero gene encodes a divergent homeodomain protein that controls neuronal identity in Drosophila. Development Suppl. 2: 79–85.

    PubMed  Google Scholar 

  • Dambly-Chaudière, C., Jamet, E., Burri, M., Bopp, D., Basier, K., Hafen, E., Dumont, N., Spielmann, P., Ghysen, A. and Noll, M. (1992) The paired box gene pox neuro: a determinant of poly-innervated sense organs in Drosophila. Cell 69: 159–172.

    Article  PubMed  Google Scholar 

  • Dobzhansky, T., Ayala, F.J., Stebbins, G.L. and Valentine, J.W. (1977) Evolution. Freeman, San Francisco.

    Google Scholar 

  • Doe, C.Q., Chu-LaGraff, Q., Wright, D.M. and Scott, M.P. (1991) The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 65: 451–464.

    Article  PubMed  CAS  Google Scholar 

  • DuLac, L., Bastiani, M.J. and Goodman, C.S. (1986) Guidance of neuronal growth cones in the grasshopper embryo: II. Recognition of a specific axonal pathway by the aCC neuron. J. Neurosci. 6: 3532–3541.

    CAS  Google Scholar 

  • Dumont, J.P.C. and Robertson, R.M. (1986) Neuronal circuits: an evolutionary perspective. Science 233: 849–853.

    Article  PubMed  CAS  Google Scholar 

  • Duncan, I. (1987) The bithorax complex. Ann. Rev. Genet. 21: 285–319.

    Article  PubMed  CAS  Google Scholar 

  • Farrel, S. and Kuhlenbeck, H. (1964) Preliminary computation of the number of cellular elements in some insect brains. Anat. Rec. 148: 369–370.

    Google Scholar 

  • Fullard, J.H. and Yack, J.E. (1993) The evolutionary biology of insect hearing. Trends Ecol. Evol. 8: 248–252.

    Article  PubMed  CAS  Google Scholar 

  • Gettrup, E. (1962) Thoracic proprioceptors in the flight system of locusts. Nature 193: 498–499.

    Article  Google Scholar 

  • Ghysen, A. (1992) The developmental biology in neuronal connectivity. Int. J. Dev. Biol. 36: 47–58.

    PubMed  CAS  Google Scholar 

  • Ghysen, A., Dambly-Chaudière, C., Aceves, E., Jan, L.Y. and Jan, Y.M. (1986) Sensory neurons and peripheral pathways in Drosophila embryos. Roux’s Arch. Dev. Biol. 195: 281–289.

    Article  Google Scholar 

  • Ghysen, A. and Dambly-Chaudière, C. (1989) Genesis of the Drosophila peripheral nervous system. Trends Genetics 5: 251–255.

    Article  CAS  Google Scholar 

  • Ghysen, A. and O’Kane, C. (1989) Neural enhancer-like elements as specific cell markers in Drosophila. Development 105: 35–52.

    CAS  Google Scholar 

  • Ghysen, A. and Dambly-Chaudière, C. (1992) Development of the peripheral nervous system in Drosophila. In: M. Shankland and E.R. Macagno (eds): Determinants of neuronal identity. Academic Press, San Diego, New York, Boston, London, Sydney, Tokyo, Toronto, pp. 226–292.

    Google Scholar 

  • Ghysen, A. and Dambly-Chaudière, C. (1993) The specification of sensory neuron identity in Drosophila. Bio Essays 15: 193–298.

    Google Scholar 

  • Giangrande, A. and Palka, J. (1990) Genes involved in the development of the peripheral nervous system of Drosophila. Seminars in Cell Biol. 1: 197–209.

    CAS  Google Scholar 

  • Goodman, C.S., Bastiani, M.J., Doe, C.Q., DuLac, S., Helfand, S.L, Kuwada, J.Y and Thomas, J.B. (1984) Cell recognition during neuronal development. Science 225: 1271–1279.

    Article  PubMed  CAS  Google Scholar 

  • Grenningloh, G., Bieber, A., Rehm, J., Snow, P.M., Traquina, Z., Hortsch, M., Patel, N.H. and Goodman, C.S. (1990) Molecular genetics of neuronal recognition in Drosophila: evolution and function of immunoglobulin superfamily cell adhesion molecules. Cold Spring Harbor Symp. Quant. Biol. 55: 327–340.

    CAS  Google Scholar 

  • Hartenstein, B. (1987) The influence of segmental compartmentalisation on the development of the larval peripheral nervous system in Drosophila melanogaster. Roux’s Arch. Dev. Biol. 196: 101–112.

    Article  Google Scholar 

  • Hartenstein, V. (1988) Development of Drosophila larval sensory organs; spatiotemporal pattern of sensory neurons, peripheral axonal pathways and sensilla differentiation. Development 102: 869–886.

    Google Scholar 

  • Heathcote, D.R. (1981) Differentiation of an identified sensory neuron (SR) and associated structures (CTO) in grasshopper embryos. J. Comp. Neurol. 202: 1–18.

    Article  PubMed  CAS  Google Scholar 

  • Ho, R.K and Goodman, C.S. (1982) Peripheral pathways are pioneered by an array of central and peripheral neurons in the grasshopper embryo. Nature 297: 404–406.

    Article  PubMed  CAS  Google Scholar 

  • Hustert, R. (1974) Morphologie und Atmungsbewegungen des 5. Abdominalsegments von Locusta migratoria. Zool. Jb. Physiol. 78: 157–174.

    Google Scholar 

  • Hustert, R. (1975) Neuromuscular coordination and proprioceptive control of rhythmical abdominal ventilation in intact Locusta migratoria. J. Comp. Physiol. 97: 159–179.

    Article  Google Scholar 

  • Jan, L.Y. and Jan, Y.N. (1982) Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and grasshopper embryos. Proc. Natl. Acad. Sci. USA 79: 2700–2704.

    Article  PubMed  CAS  Google Scholar 

  • Jan, Y.N. and Jan, L.Y. (1990) Genes required for specifying cell fates in Drosophila embryonic sensory nervous system. Trends Neurosci. 13: 493–498.

    Article  PubMed  CAS  Google Scholar 

  • Jarman, A.P., Grau, Y., Jan, L.Y., and Jan, Y.N. (1993) atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73: 1307–1321.

    Article  PubMed  CAS  Google Scholar 

  • Karch, F., Bender, W. and Wehffenbach, B. (1990) abdA expression in Drosophila embryos. Genes Dev. 4: 1573–1587.

    Article  PubMed  CAS  Google Scholar 

  • Keshishian, H. and Bentley, D. (1983a) Embryogenesis of peripheral nerve pathways in grasshopper legs. I. The initial nerve pathway to the CNS. Dev. Biol. 96: 89–102.

    Article  PubMed  CAS  Google Scholar 

  • Keshishian, H. and Bentley, D. (1983b) Embryogenesis of peripheral nerve pathways in grasshopper legs. II. The major nerve roots. Dev. Biol. 96: 103–115.

    Article  PubMed  CAS  Google Scholar 

  • Kristensen, N.P. (1981) Phylogeny of insect orders. Ann. Rev. Entomol. 26: 135–157.

    Article  Google Scholar 

  • Lakes-Harlan, R. and Pollack, G.S. (1993) Pathfinding of peripheral neurons in the central nervous system of an embryonic grasshopper (Chorthippus biguttulus). Cell Tissue Res. 237: 97–106.

    Article  Google Scholar 

  • Matsuda, R. (1976) Morphology and evolution of the insect abdomen. Pergamon Press, New York.

    Google Scholar 

  • Meier, T. and Reichert, H. (1990) Embryonic development and evolutionary origin of the Orthopteran auditory organs. J. Neurobiol. 21: 592–610.

    Article  PubMed  CAS  Google Scholar 

  • Meier T. and Reichert, H. (1991) Serially homologous development of the peripheral nervous system in the mouthparts of the grasshopper. J. Comp. Neurol. 305: 201–214.

    Article  PubMed  CAS  Google Scholar 

  • Meier, T., Chabaud, F. and Reichert, H. (1991) Homologous patterns in the embryonic development of the peripheral nervous system in the grasshopper Schistocerca gregaria and the fly Drosophila melanogaster. Development 112: 241–253.

    CAS  Google Scholar 

  • Nottebohm, E., Dambly-Chaudière, C and Ghysen, A. (1992) Connectivity of chemosensory neurons is controlled by the gene poxn in Drosophila. Nature 359: 829–832.

    CAS  Google Scholar 

  • Nottebohm, E., Usui, A., Therianos, S., Kimura, K., Dambly-Chaudière, C and Ghysen, A. (1994) The gene poxn controls different steps of the formation of chemosensory organs in Drosophila. Neuron 12: 25–34.

    CAS  Google Scholar 

  • Pearson, K.G., Hedwig, B. and Wolf, H. (1989) Are the hindwing chordotonal organs elements of the locust flight pattern generator? J. Exp. Biol. 114: 235–255.

    Google Scholar 

  • Pearson, K.G., Boyan, G.S., Bastiani, M. and Goodman, C.S. (1985) Heterogeneous properties of segmentally homologous interneurons in the ventral nerve cord of locusts. J. Comp. Neurol. 233: 133–145.

    Article  PubMed  CAS  Google Scholar 

  • Pfeifer, M., Karch, F. and Bender, W. (1987) The bithorax complex: control of segmental identity. Genes Dev. 1: 891–898.

    Article  Google Scholar 

  • Raff, R.A. and Kaufmann, T.C. (1983) Embryos, genes and evolution. Macmillan, New York.

    Google Scholar 

  • Reichert, H. (1994) Molecular correlates of neuronal specificity in the developing insect nervous system. Mol. Neurobiol. 7: 349–362.

    Article  Google Scholar 

  • Robertson, R.M., Pearson, K.G. and Reichert, H. (1982) Flight interneurons in the locust and the origin of insect wings. Science 217: 177–179.

    Article  PubMed  CAS  Google Scholar 

  • Roth, V.L. (1984) On homology. Biol. J. Linn. Soc. 22: 13–29.

    Article  Google Scholar 

  • Sander, K. (1988) Studies in insect segmentation: from teratology to phenogenetics. Development (Suppl) 104: 112–121.

    Google Scholar 

  • Tear, G., Bate, C.M. and Martinez-Arias, A. (1988) A phylogenetic interpretation of the patterns of gene expression in Drosophila embryos. Development (Suppl.) 104: 135–145.

    Google Scholar 

  • Thomas, J.B., Bastiani, M.J., Bate M. and Goodman, C.S. (1984) From grasshopper to Drosophila: a common plan for neuronal development. Nature 310: 203–207.

    Article  PubMed  CAS  Google Scholar 

  • Uemura, T., Shepherd, S., Ackerman, L., Jan, L.Y. and Jan, Y.N. (1989) numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 58: 349–360.

    Article  PubMed  CAS  Google Scholar 

  • Vaessin, H., Grell, E., Wolff, E., Bier, E., Jan, L.Y. and Jan Y.M. (1991) prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell 67: 941–953.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, J.A., Phillips, C.E., Adams, M.W. and Huber, F. (1982) Structural comparison of a homologous neuron in Gryllid and Acridid insects. J. Neurobiol. 13: 459–468.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, G.P. (1989) The biological homology concept. Annu. Rev. Eco. Syst. 20: 51–69.

    Article  Google Scholar 

  • Whitington, P.M. (1989) The early development of motor axon pathways in the locust: the establishment of the segmental nerves in the thoracic ganglia. Development 105: 715–721.

    Google Scholar 

  • Whitlock, K.E. (1993) Development of Drosophila wing sensory neurons in mutants with missing or modified cell surface molecules. Development 117: 1251–1260.

    PubMed  CAS  Google Scholar 

  • Yack, J.E. and Fullard, J. H. (1990) The mechanoreceptive origin of insect tympanal organs: A comparative study of similar nerves in tympanate and atympanate moths. J. Comp. Neurol. 300: 523–534.

    Article  PubMed  CAS  Google Scholar 

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Meier, T., Reichert, H. (1995). Developmental mechanisms, homology and evolution of the insect peripheral nervous system. In: Breidbach, O., Kutsch, W. (eds) The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach. Experientia Supplementum, vol 72. Birkhäuser Basel. https://doi.org/10.1007/978-3-0348-9219-3_12

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  • DOI: https://doi.org/10.1007/978-3-0348-9219-3_12

  • Publisher Name: Birkhäuser Basel

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