In female grasshoppers, oviposition is a highly specialized behavior involving a rhythm-generating neural circuit, the oviposition central pattern generator, unusual abdominal appendages, and dedicated muscles. This study of Schistocerca americana (Drury) grasshoppers was undertaken to determine whether the simpler pregenital abdominal segments, which do not contain ovipositor appendages, share common features with the genital segment, suggesting a roadmap for the genesis of oviposition behavior. Our study revealed that although 5 of the standard pregenital body wall muscles were missing in the female genital segment, homologous lateral nerves were, indeed, present and served 4 ovipositor muscles. Retrograde labeling of the corresponding pregenital nerve branches in male and female grasshoppers revealed motor neurons, dorsal unpaired median neurons, and common inhibitor neurons which appear to be structural homologues of those filled from ovipositor muscles. Some pregenital motor neurons displayed pronounced contralateral neurites; in contrast, some ovipositor motor neurons were exclusively ipsilateral. Strong evidence of structural homology was also obtained for pregenital and ovipositor skeletal muscles supplied by the identified neurons and of the pregenital and ovipositor skeletons. For example, transient embryonic segmental appendages were maintained in the female genital segments, giving rise to ovipositor valves, but were lost in pregenital abdominal segments. Significant proportional differences in sternal apodemes and plates were observed, which partially obscure the similarities between the pregenital and genital skeletons. Other changes in reorganization included genital muscles that displayed adult hypertrophy, 1 genital muscle that appeared to represent 2 fused pregenital muscles, and the insertion points of 2 ovipositor muscles that appeared to have been relocated. Together, the comparisons support the idea that the oviposition behavior of genital segments is built upon a homologous, segmentally iterated motor infrastructure located in the pregenital abdomen of male and female grasshoppers.

Keywords:
Grasshopper, Oviposition, Abdominal motor system
1.
Albrecht FO (1953): The Anatomy of the Migratory Locust. London, Athlone Press.
2.
Arbas EA (1983): Neural correlates of flight loss in a Mexican grasshopper, Barytettix psolus. 1. Motor and sensory cells. J Comp Neurol 216:369-380.
3.
Arbas EA, Meinertzhagen IA, Shaw SR (1991): Evolution in nervous systems. Annu Rev Neurosci 14:9-38.
4.
Ayali A, Lange AB (2010): Rhythmic behaviour and pattern-generating circuits in the locust: key concepts and recent updates. J Insect Physiol 56:834-843.
5.
Bentley D, Keshishian H, Shankland M, Toroian-Raymond A (1979): Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. J Embryol Exp Morphol 54:47-74.
6.
Berkowitz A (2008): Physiology and morphology of shared and specialized spinal interneurons for locomotion and scratching. J Neurophysiol 99:2887-2901.
7.
Breidbach O, Kutsch W (1990): Structural homology of identified motoneurones in larval and adult stages of hemi- and holometabolous insects. J Comp Neurol 297:392-409.
8.
Burrows M, Bevan S (1999): Maps of the somata of efferent neurons with axons in the lateral nerves of locust abdominal ganglia. J Exp Biol 202:2911-2923.
9.
Cangliano L, Hill RH, Grillner S (2012): The hemi-segmental locomotor network revisited. Neurosci 210:33-37.
10.
Da Silva R, Lange AB (2011): Evidence of a central pattern generator regulating spermathecal muscle activity in Locusta migratoria and its coordination with oviposition. J Exp Biol 214:757-763.
11.
Edwards JS, Palka J (1991): Insect neural evolution - a fugue or an opera? Sem Neurosci 3:391-398.
12.
Ferber M, Pfluger H-J (1990): Bilaterally projecting neurons in pregenital abdominal ganglia of the locust: anatomy and peripheral targets. J Comp Neurol 302:447-460.
13.
Ficcapointe G, Lange AB (1996): Control of the motor pattern generator in the VIIth abdominal ganglion of Locusta: descending neural inhibition and coordination with the oviposition hole digging central pattern generator. J Insect Physiol 42:791-798.
14.
Fuchs E, Hulata E, Ben-Jacob E, Ayali A (2006): Adult, sex-specific behavior characterized by elevated neuronal functional complexity. Neuroreport 17:1153-1158.
15.
Goodman CS, Bate M (1981): Neuronal development in the grasshopper. Trends Neurosci 4:103-169.
16.
Grillner S (2003): The motor infrastructure; from ion channels to neuronal networks. Nat Rev Neurosci 4:573-586.
17.
Grillner S (2006): Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751-766.
18.
Jarvis E, Bruce HS, Patel NH (2012): Evolving specialization of the arthropod nervous system. Proc Natl Acad Sci USA 109:10634-10639.
19.
Jorgensen WK, Rice MJ (1983): Superextension and supercontraction in locust ovipositor muscles. J Insect Physiol 29:427-448.
20.
Kalogianni E (1996): Morphology and physiology of abdominal projection interneurons in the locust with mechanosensory inputs for ovipositor hair receptors. J Comp Neurol 366:656-673.
21.
Katz PS (2010): Comparative studies provide evidence for neural reuse. Behav Brain Res 33:278-279.
22.
Katz PS, Harris-Warrick RM (1999): The evolution of neuronal circuits underlying species-specific behavior. Curr Opin Neurobiol 9:628-633.
23.
Katz PS, Newcomb JM (2006): A tale of two CPGs: phylogenetically polymorphic networks; in Kaas JH (ed): Evolution of Nervous Systems: a Comprehensive Reference. Oxford, Elsevier, pp 367-374.
24.
Kutsch W, Heckmann R (1995): Motor supply of the dorsal longitudinal muscles. 1. Homonomy and ontogeny of the motoneurones in locusts (Insecta, Caelifera). Zoomorphology 115:179-195.
25.
Lange AB, Orchard I, Loughton BG (1984): Neural inhibition of egg-laying in the locust Locusta migratoria. J Insect Physiol 30:271-278.
26.
Lewis GW, Miller PL, Mills PS (1973): Neuro-muscular mechanisms of abdominal pumping in the locust. J Exp Biol 59:149-168.
27.
Matsuda R (1976): Morphology and Evolution of the Insect Abdomen. New York, Pergamon Press.
28.
McKenna KE, Chung SK, McVary KT (1991): A model for the study of sexual function in anesthetized male and female rats. Am J Physiol 261:1276-1285.
29.
Meier T, Chabaud F, 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.
30.
Meier T, Reichert H (1990): Embryonic development and evolutionary origin of the orthopteran auditory organs. J Neurobiol 21:2592-2610.
31.
Meier T, Reichert H (2004): Serially homologous development of the peripheral nervous system in the mouthparts of the grasshopper. J Comp Neurol 305:201-214.
32.
Newcomb JM, Katz PS (2009): Different functions for homologous serotonergic interneurons and serotonin in species-specific rhythmic behaviours. Proc Biol Sci 276:99-108.
33.
Newland PL, Yates P (2008): Contact chemoreception in egg-laying behavior of locusts. J Insect Physiol 54:273-285.
34.
Niven JE, Graham CM, Burrows M (2008): Diversity and evolution of the insect ventral nerve cord. Ann Rev Entomol 53:253-271.
35.
Paul DH (2004): Projection and local interneurons in the sixth abdominal ganglion of the sand crab Emerita analoga (Hippidae). J Comp Neurol 480:253-271.
36.
Qadri MAH (1940): On the development of the genitalia and their ducts in Orthopteroid insects. Trans R Ent Soc Lond 90:121-175.
37.
Rast GF, Braunig P (2001): Insect mouthpart motor patterns: central circuits modified for highly derived appendages? Neurosci 108:167-176.
38.
Rose U (2004): Morphological and functional maturation of a skeletal muscle regulated by juvenile hormone. J Exp Biol 207:483-495.
39.
Rose U, Ferber M, Hustert R (2001): Maturation of muscle properties and its hormonal control in an adult insect. J Exp Biol 206:445-455.
40.
Ryczko D, Dubuc R, Cabelquen JM (2010): Rhythmogenesis in axial locomotor circuits: an interspecies comparison. Prog Brain Res 187:189-211.
41.
Schmah M, Wolf H (2003): Inhibitory motor neurons supply body wall muscles in the locust abdomen. J Exp Biol 206:445-455.
42.
Schmitt JB (1954): The nervous system of the pregenital abdominal segments of some orthoptera. Ann Entomol Soc Am 47:677-682.
43.
Seabrooke WD (1968): The innervation of the terminal abdominal segments (VIII-XI) of the desert locust, Schistocerca gregaria. Can Ent 100:693-715.
44.
Sink H, Whittington PM (1991): Pathfinding in the central nervous system and periphery by identified embryonic Drosophila motor axons. Development 112:307-316.
45.
Snodgrass RE (1935): The abdominal mechanisms of a grasshopper. Smithson Misc Collect 94:1-89.
46.
Steffens G, Kutsch W, Xie F, Reichert H (1995): Segmental differentiation processes in embryonic muscle development of the grasshopper. Dev Genes Evol 204:453-464.
47.
Stephenson-Jones M, Ericsson J, Robertson B, Grillner S (2012): Evolution of the basal ganglia: dual-output pathways conserved throughout vertebrate phylogeny. J Comp Neurol 520:2975-2973.
48.
Technau GM, Berger C, Urbach R (2005): Generation of cell diversity and segmental pattern in the embryonic central nervous system of Drosophila. Dev Dyn 235:861-869.
49.
Thomas JB, Bastiani MJ, Bate M, Goodman CS (1984): From grasshopper to Drosophila: a common plan for neuronal development. Nature 310:203-207.
50.
Thompson KJ (1986a): Oviposition digging in the grasshopper. 1. Functional anatomy and the motor programme. J Exp Biol 122:387-411.
51.
Thompson KJ (1986b): Oviposition digging in the grasshopper. 2. Descending neural control. J Exp Biol 122:413-425.
52.
Thompson KJ, Roosevelt JL (1998): Comparison of neural elements in sexually dimorphic segments of the grasshopper, Schistocerca americana. J Comp Neurol 394:14-28.
53.
Thompson KJ, Siegler MVS (1991): Anatomy and physiology of spiking local and intersegmental interneurons in the median neuroblast lineage of the grasshopper. J Comp Neurol 305:659-675.
54.
Thompson KJ, Sivanesan SP, Campbell HR, Sanders KA (1999): Efferent neurons and specialization of abdominal segments in grasshoppers. J Comp Neurol 415:65-79.
55.
Tousson E, Hustert R (2000): Central projections from contact chemoreceptors of the locust ovipositor and adjacent cuticle. Cell Tissue Res 302:285-294.
56.
Truman JW, Ball EE (1998): Patterns of embryonic neurogenesis in a primitive wingless insect, the silverfish, Ctenolepisma longicaudata: comparison with those seen in flying insects. Dev Genes Evol 208:357-368.
57.
Vincent JFV (1976): How does the female locust dig her oviposition hole? J Entomol 50:175-181.
58.
Wallis EJ, Paul DH, Antonsen BL, Hollenberg R (1995): Variations on a segmental theme: muscle receptor organs and extensor neuromusculature in the squat lobster Munida quadrispina (Anomura, Galatheidae). J Exp Biol 198:2453-2463.
59.
Wanischeck M, Rose U (2005): Unusual tension reception in an insect. J Neurobiol 65:115-124.
60.
Whiting MF, Bradler S, Maxwell T (2003): Loss and recovery of wings in stick insects. Nature 421:264-267.
61.
Xie F, Meier T, Reichert H (1992): Embryonic development of muscle patterns in the body wall of the grasshopper. Roux's Arch Dev Biol 201:301-311.
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