Muscle development in the grasshopper embryo. I. Muscles, nerves, and apodemes in the metathoracic leg.

Much is known about the development of nerve pathways in the metathoracic limb bud of the grasshopper embryo. In this series of three papers, we report on the development of muscles in the same embryonic appendage. In a fourth paper (E. E. Ball, R. K. Ho, and C. S. Goodman, 1985, J. Neurosci, in press) we examine the development of specific neuromuscular connections for one of these muscles (coxal muscle 133a). In this first paper, we present an overview of the development of muscles, nerves, and apodemes (tendons). We previously reported on a class of large mesodermal cells, called muscle pioneers (MPs), that arises early in development and appears to act as a scaffold for developing muscles and guidance cue for motoneuron growth cones (R. K. Ho, E. E. Ball, and C. S. Goodman, 1983, Nature (London) 301, 66-69). We have used the I-5 monoclonal antibody (which specifically labels the MPs as well as the nerve pathways), HRP immunocytochemistry, and Normarski optics to visualize muscle, nerve, and apodeme development in the embryonic metathoracic limb bud from 27.5% (before the appearance of the MPs) to 55% (after the muscles have attained their basic adult pattern). Cell fusions, cell migration, and cell death all appear to play important roles in the development of MPs. The patterns of muscle development vary greatly, ranging from (i) single MPs for simple muscles (which in the adult have only one bundle of muscle fibers, e.g., coxal muscle 133a), to (ii) arrays of MPs for complex muscles [which in the adult have many bundles of muscle fibers each with separate sites of insertion, e.g., the extensor tibiae (ETi) and flexor tibiae (FlTi) muscles in the femur].

[1]  R. Ho,et al.  Guidance of pioneer growth cones: filopodial contacts and coupling revealed with an antibody to Lucifer Yellow. , 1982, Developmental biology.

[2]  M. Burns,et al.  Mechanical properties of locust extensor tibiae muscles , 1978 .

[3]  A. Crossley Ultrastructural changes during transition of larval to adult intersegmental muscle at metamorphosis in the blowfly Calliphora erythrocephala. I. Dedifferentiation and myoblast fusion. , 1972, Journal of embryology and experimental morphology.

[4]  H. Keshishian,et al.  Pioneer neurons and pathways in insect appendages , 1982, Trends in Neurosciences.

[5]  Axon growth from limb motoneurons in the locust embryo: the effect of target limb removal on the path taken out of the central nervous system. , 1982, Developmental biology.

[6]  A. Kammer,et al.  Comparison of slow larval and fast adult muscle innervated by the same motor neurone. , 1980, The Journal of experimental biology.

[7]  Graham Hoyle,et al.  Muscles and their neural control , 1983 .

[8]  T. Sahota,et al.  ORIENTATION DETERMINATION OF DEVELOPING FLIGHT MUSCLES IN GALLERIA MELLONELLA , 1967 .

[9]  J. Truman,et al.  Peptide and steroid regulation of muscle degeneration in an insect. , 1982, Science.

[10]  Christine E. Phillips,et al.  An Arthropod Muscle Innervated by Nine Excitatory Motor Neurones , 1980 .

[11]  A. Kammer,et al.  Structural and electrotonic connections between developing moth muscle fibers. , 1982, Journal of neurobiology.

[12]  R. Ho,et al.  Peripheral pathways are pioneered by an array of central and peripheral neurones in grasshopper embryos , 1982, Nature.

[13]  Identified neurons in an insect embryo: The pattern of neurons innervating the metathoracic leg of the locust , 1981, The Journal of comparative neurology.

[14]  J. Denburg,et al.  Formation of the leg neuromuscular system in embryos of the cockroach, Periplaneta americana: I. Light microscope studies , 1982 .

[15]  H. L. Carson,et al.  The Genetics and Biology of Drosophila , 1976, Heredity.

[16]  Bate Cm Pioneer neurones in an insect embryo. , 1976 .

[17]  L. E. Chadwick,et al.  THE EMBRYONAL AND NYMPHAL CERVICOTHORACIC MUSCULATURE OF THE AMERICAN COCKROACH, PERIPLANETA AMERICANA (BLATTARIA: BLATTIDAE) , 1967, The Canadian Entomologist.

[18]  R. Ho,et al.  Muscle pioneers: large mesodermal cells that erect a scaffold for developing muscles and motoneurones in grasshopper embryos , 1983, Nature.

[19]  A. Crossley The fine structure and mechanism of breakdown of larval intersegmental muscles in the blowfly Calliphora erythrocephala , 1968 .

[20]  G Hoyle,et al.  Neural mechanism underlying behavior in the locust Schistocerca gregaria. 3. Topography of limb motorneurons in the metathoracic ganglion. , 1973, Journal of neurobiology.

[21]  A. Crossley Transformations in the abdominal muscles of the blue blow-fly, Calliphora erythrocephala (Meig), during metamorphosis. , 1965, Journal of embryology and experimental morphology.

[22]  Pattern regulation of mesoderm in transplanted and supernumerary limbs of the cockroach. II. Time course of muscle dedifferentiation , 1980 .

[23]  J. Nardi Induction of invagination in insect epithelium: paradigm for embryonic invagination. , 1981, Science.

[24]  A. Crossley Ultrastructural changes during transition of larval to adult intersegmental muscle at metamorphosis in the blowfly Calliphora erythrocephala. II. The formation of adult muscle. , 1972, Journal of embryology and experimental morphology.

[25]  W. J. Heitler The Locust Jump: III. Structural Specializations of the Metathoracic Tibiae , 1977 .

[26]  O. W. Tiegs The flight muscles of insects-their anatomy and histology; with some observations on the structure of striated muscle in general , 1955, Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences.

[27]  C Q Doe,et al.  Early events in insect neurogenesis. II. The role of cell interactions and cell lineage in the determination of neuronal precursor cells. , 1985, Developmental biology.

[28]  Muscle development in the grasshopper embryo. III. Sequential origin of the flexor tibiae muscle pioneers. , 1985, Developmental biology.

[29]  Selective groups of neuronal and mesodermal cells recognized early in grasshopper embryogenesis by a monoclonal antibody. , 1983, Brain research.

[30]  N. Tyrer Functional development of the reticular system in an insect muscle with synchronously differentiating cells. , 1973, Journal of cell science.

[31]  Michael Bate,et al.  Neuronal development in the grasshopper , 1981, Trends in Neurosciences.

[32]  H. Keshishian,et al.  Embryogenesis of peripheral nerve pathways in grasshopper legs. III. Development without pioneer neurons. , 1983, Developmental biology.

[33]  Organization of motor neurons to a multiply innervated insect muscle. , 1981, Journal of neurobiology.

[34]  G. Hoyle,et al.  The anatomy and innervation of locust skeletal muscle , 1955, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[35]  Usherwood Pn,et al.  Physiology and Ultrastructure of Phasic and Tonic Skeletal Muscle Fibres in the Locust, Schistocerca Gregaria , 1972 .

[36]  Embryogenesis of peripheral nerve pathways in grasshopper legs. II. The major nerve routes. , 1983, Developmental biology.

[37]  P. Usherwood AMINO-ACID GATED ION CHANNELS IN LOCUST MUSCLE MEMBRANE , 1981 .

[38]  G. Williams,et al.  A gradient of morphogenetic information involved in muscle patterning. , 1980, Journal of embryology and experimental morphology.

[39]  F. Crick,et al.  A gradient of positional information in an insect, Rhodnius. , 1972, Journal of cell science.

[40]  T. Reese,et al.  Three-dimensional structure and membrane specializations of moth excitatory neuromuscular synapse. , 1978, Journal of ultrastructure research.

[41]  R. Miledi,et al.  Properties of miniature excitatory junctional currents at the locust nerve‐muscle junction , 1982, The Journal of physiology.

[42]  R. Snodgrass The thoracic mechanism of a grasshopper, and its antecedents , 1929 .

[43]  W. J. Heitler,et al.  The locust jump. II. Neural circuits of the motor programme. , 1977, The Journal of experimental biology.

[44]  T. Sahota,et al.  THE INFLUENCE OF EPIDERMIS ON THE DEVELOPING FLIGHT MUSCLES IN GALLERIA MELLONELLA , 1967 .

[45]  M. Titmus Ultrastructure of identified fast excitatory, slow excitatory and inhibitory neuromuscular junctions in the locust , 1981, Journal of neurocytology.

[46]  G A Horridge,et al.  The organization of inputs to motoneurons of the locust metathoracic leg. , 1974, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[47]  H. Keshishian,et al.  Pathfinding by Peripheral Pioneer Neurons in Grasshoppers , 1982, Science.

[48]  W. J. Heitler,et al.  The locust jump. I. The motor programme. , 1977, The Journal of experimental biology.

[49]  H. Keshishian,et al.  Embryogenesis of peripheral nerve pathways in grasshopper legs. I. The initial nerve pathway to the CNS. , 1983, Developmental biology.

[50]  C. Goodman,et al.  Guidance of Peripheral Pioneer Neurons in the Grasshopper: Adhesive Hierarchy of Epithelial and Neuronal Surfaces , 1984, Science.

[51]  J. Whittaker,et al.  Developmental autonomy of muscle fine structure in muscle lineage cells of ascidian embryos. , 1983, Developmental biology.

[52]  R. Snodgrass,et al.  Principles of Insect Morphology , 1993 .

[53]  C. Goodman,et al.  Muscle development in the grasshopper embryo. II. Syncytial origin of the extensor tibiae muscle pioneers. , 1985, Developmental biology.

[54]  C. Goodman,et al.  Transient expression of a surface antigen on a small subset of neurones during embryonic development , 1984, Nature.

[55]  G Hoyle,et al.  Distributions of nerve and muscle fibre types in locust jumping muscle. , 1978, The Journal of experimental biology.

[56]  J. A. Wilson,et al.  The structure and function of serially homologous leg motor neurons in the locust. I. Anatomy. , 1979, Journal of neurobiology.

[57]  M J Bastiani,et al.  Pathfinding by neuronal growth cones in grasshopper embryos. IV. The effects of ablating the A and P axons upon the behavior of the G growth cone , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[58]  H. Keshishian The origin and morphogenesis of pioneer neurons in the grasshopper metathoracic leg. , 1980, Developmental biology.

[59]  A. Kammer,et al.  Membrane structures and physiology of an immature synapse , 1981, Journal of neurocytology.

[60]  Neuronal growth cones: specific interactions mediated by filopodial insertion and induction of coated vesicles. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[61]  M. Burns,et al.  The Control of Walking in Orthoptera: II. Motor Neurone Activity in Normal Free-Walking Animals , 1979 .

[62]  J. Truman,et al.  Cell death in invertebrate nervous systems. , 1984, Annual review of neuroscience.

[63]  M. O'Shea,et al.  The identification of an octopaminergic neurone and the modulation of a myogenic rhythm in the locust. , 1978, The Journal of experimental biology.

[64]  David Bentley,et al.  Pioneer axons lose directed growth after selective killing of guidepost cells , 1983, Nature.