Summary
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1.
The giant Madagascar cockroach,Gromphadorhina portentosa, hisses by expelling air from a pair of specialized abdominal spiracles. The anatomy and innervation of serially homologous respiratory and sound-producing spiracles were compared in order to determine the evolutionary steps by which a new behavior has developed.
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2.
The trachea leading to the sound-producing (fourth) spiracle shows a constriction proximally; distally it is greatly elongated with a conical bore (Fig. 2). These features, which are lacking in other spiracles, are sufficient to account for the character of the sound (Fig. 10).
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3.
The motoneurons innervating both types of spiracles were located by axonal diffusion of cobalt, and their morphology was determined in wholemounted ganglia. The number, ganglionic locations, and in some cases branching patterns of motoneurons serving the sound-producing and respiratory spiracles were essentially identical (Figs. 4, 5, 6).
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4.
Physiological activity was recorded along spiracle nerves and within spiracle muscle fibers; four units were identified for each spiracle, agreeing with the number of cells located anatomically. These included, for each abdominal spiracle, an opener exciter motoneuron, two closer exciter motoneurons, and one closer inhibitor motoneuron (Figs. 7, 8).
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5.
During normal respiration the output of these 4 units had similar phase relationships in all abdominal spiracles which were examined; lower firing rates in the motoneurons innervating the hissing spiracles rendered these nonfunctional during normal respiration (Fig. 9).
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6.
The findings are consistent with conservation of motor innervation and of central pattern generators during evolution.
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Abbreviations
- AI :
-
first abdominal ganglion
- AII :
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second abdominal ganglion
- MNHO :
-
median neurohaemal organ
- N2 :
-
first segmentai root (abdominal ganglia)
- TI :
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first thoracic ganglion
- TIII :
-
third thoracic ganglion
References
Altman, J.S., Tyrer, N.M.: Insect flight as a system for the study of the development of neuronal connections. In: Experimental analysis of insect behaviour. Barton Browne, L. (ed.), pp. 159–179. Berlin, Heidelberg, New York: Springer 1974
Bacon, J.P., Altman, J.S.: A silver intensification method for cobalt-filled neurones in wholemount preparations. Brain Res.138, 359–363 (1977)
Bentley, D.R.: Genetic control of an insect neuronal network. Science174, 1139–1141 (1971)
Bentley, D.R.: Postembryonic development of insect motor systems. In: Developmental neurobiology of arthropods. Young, D. (ed.), pp. 147–177. Cambridge: Cambridge University Press 1973
Bentley, D.R., Hoy, R.R.: Postembryonic development of adult motor patterns in crickets: a neural analysis. Science170, 1409–1411 (1970)
Case, J.F.: The median nerves and cockroach spiracular function. J. Insect Physiol.1, 85–94 (1957)
Dumortier, B.: L'émission sonore dans le genreGromphadorhina brunner (Blattodea, Perisphaeriidae), étude morphologique et biologique. Bull. Soc. Zool. France90, 89–101 (1965)
Eisner, T.: Spray mechanism of the cockroachDiploptera punctata. Science128, 148–149 (1958)
Evans, P.D.: The uptake ofl-glutamate by the central nervous system of the cockroach,Periplaneta americana. J. Exp. Biol.62, 55–67 (1975)
Goodman, C.S.: Neuron duplications and deletions in locust clones and clutches. Science197, 1384–1386 (1977)
Hoy, R.R., Hahn, J., Paul, R.C.: Hybrid cricket auditory behavior: evidence for genetic coupling in animal communication. Science195, 82–84 (1977)
Kammer, A.E., Rheuben, M.B.: Adult motor patterns produced by moth pupae during development. J. Exp. Biol.65, 65–84 (1976)
Levi-Montalcini, R., Chen, J.S., Seshan, K.R., Aloe, L.: An invitro approach to the insect nervous system. In: Developmental neurobiology of arthropods. Young, D. (ed.), pp. 5–36. Cambridge: Cambridge University Press 1973
Lewis, D.B.: The physiology of the Tettigoniid ear. I. The implication of the anatomy of the ear to its function in sound reception. J. Exp. Biol.60, 821–837 (1974)
Lighthill, M.J.: On sound generated aerodynamically. I. General theory. Proc. R. Soc. Lond. A211, 564–587 (1952)
Miller, P.L.: Inhibitory nerves to insect spiracles. Nature (Lond.)221, 171–173 (1969)
Miller, P.L.: Spatial and temporal changes in the coupling of cockroach spiracles to ventilation. J. Exp. Biol.59, 137–148 (1973)
Miller, P.L.: Respiration-aerial gas transport. In: The physiology of insecta, 2nd ed., Vol. VI. Rockstein, M. (ed.), pp. 345–502. New York, London: Academic Press 1974
Morse, A.P.: Further researches on North American Acridiidae. Publ. Carnegie Inst. Wash.68, 3–54 (1907)
Nelson, M.C., Fraser, J.: Sound production in the cockroach,Gromphadorhina portentosa: Evidence for communication by hissing, (in preparation)
Nocke, H.: Physical and physiological properties of the Tettigoniid (“grasshopper”) ear. J. Comp. Physiol.100, 25–57 (1975)
Pearson, K.G., Bergman, S.J.: Common inhibitory motoneurones in insects. J. Exp. Biol.50, 445–471 (1969)
Pitman, R.M., Tweedle, C.D., Cohen, M.J.: Branching of central neurons: intracellular cobalt injection for light and electron microscopy. Science176, 412–414 (1972)
Roederer, J.G.: Introduction to the physics and psychophysics of music (ed. 2). Berlin, Heidelberg, New York: Springer 1975
Roth, L.M., Stay, B.: The occurrence of para-quinones in some arthropods, with emphasis on the quinone-secreting tracheal glands ofDiploptera punctata (Blattaria). J. Insect Physiol.1, 305–318 (1958)
Shankland, D.L.: Nerves and muscles of the pregenital abdominal segments of the American cockroach,Periplaneta americana (L.). J. Morph.117, 353–386 (1965)
Simmons, P.: The neuronal control of dragonfly flight I. Anatomy. J. Exp. Biol.71, 123–140 (1977)
Strausfeld, N.J., Obermayer, M.: Resolution of intraneuronal and transynaptic migration of cobalt in the insect visual and central nervous systems. J. Comp. Physiol.110, 1–12 (1976)
Taylor, H.M., Truman, J.W.: Metamorphosis of the abdominal ganglia of the tobacco hornworm,Manduca sexta. J. Comp. Physiol.90, 367–388 (1974)
Truman, J.W.: Development and hormonal release of adult behavior patterns in silkmoths. J. Comp. Physiol.107, 39–48 (1976)
Truman, J.W., Reiss, S.E.: Dendritic reorganization of an identified motoneuron during metamorphosis of the tobacco hornworm moth. Science192, 477–479 (1976)
Tyrer, N.M., Bell, E.M.: The intensification of cobalt-filled neurone profiles using a modification of Timm's sulphide-silver method. Brain Res.73, 151–155 (1974)
Willows, A.O.D., Dorsett, D.A.: Evolution of swimming behavior inTritonia and its neurophysiological correlates. J. Comp. Physiol.100, 117–133 (1975)
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I wish to thank S. Camazine, J. Gagliardi, J. LaFratta, W. Dragun, M. LaFratta, and S. Wilson for their expert technical assistance. Drs. B. Campenot, J. Hildebrand, S. Matsumoto, D. Potter and L. Tolbert provided valuable comments on the manuscript. Dr. L. Roth supplied the original specimens ofG. portentosa. I am especially grateful to Dr. J. G. Hildebrand for providing facilities for these experiments. This research was supported by NSF grant BNS 76-81929 to MCN and JGH, NIH grant NS-11010 to JGH, and a grant from the Milton Fund of Harvard University; the author was supported by NIH training grants NS-05731 and NS-07009.
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Nelson, M.C. Sound production in the cockroach,Gromphadorhina portentosa: The sound-producing apparatus. J. Comp. Physiol. 132, 27–38 (1979). https://doi.org/10.1007/BF00617729
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DOI: https://doi.org/10.1007/BF00617729