Comparative Neuroanatomy of the Mechanosensory Subgenual Organ Complex in the Peruvian Stick Insect, Oreophoetes peruana

Abstract

The subgenual organ complex in the leg of Polyneoptera (Insecta) consists of several chordotonal organs specialized to detect mechanical stimuli from substrate vibrations and airborne sound. In stick insects (Phasmatodea), the subgenual organ complex contains the subgenual organ and the distal organ located distally to the subgenual organ. The subgenual organ is a highly sensitive detector for substrate vibrations. The distal organ has a characteristic linear organization of sensilla and likely also responds to substrate vibrations. Despite its unique combination of sensory organs, the neuroanatomy of the subgenual organ complex of stick insects has been investigated for only very few species so far. Phylogenomic analysis has established for Phasmatodea the early branching of the sister groups Oriophasmata, the Old World phasmids, and Occidophasmata, the New World phasmids. The species studied for the sensory neuroanatomy, including the Indian stick insect Carausius morosus, belong to the Old World stick insects. Here, the neuroanatomy of the subgenual organ complex is presented for a first species of the New World stick insects, the Peruvian stick insect Oreophoetes peruana. To document the sensory organs in the subgenual organ complex and their innervation pattern, and to compare these between females and males of this species and also to the Old World stick insects, axonal tracing is used. This study documents the same sensory organs for O. peruana, subgenual organ and distal organ, as in other stick insects. Between the sexes of this species, there are no notable differences in the neuroanatomy of their sensory organs. The innervation pattern of tibial nerve branches in O. peruana is identical to other stick insect species, although the innervation pattern of the subgenual organ by a single tibial nerve branch is simpler. The shared organization of the organs in the subgenual organ complex in both groups of Neophasmatodea (Old World and New World stick insects) indicates the sensory importance of the subgenual organ but also of the distal organ. Some variation exists in the innervation of the chordotonal organs in O. peruana though a common innervation pattern can be identified. The findings raise the question for the ancestral neuroanatomical organization and innervation in stick insects.

© 2022 The Author(s). Published by S. Karger AG, Basel

References Albert JT, Göpfert MC. Hearing in Drosophila. Curr Opin Neurobiol. 2015;34:79–85. Attygalle AB, Hearth KB, Iyengar VK, Morgan RC. Biosynthesis of Quinoline by a stick insect. J Nat Prod. 2021;84(2):527–30. Ball EE, Field LH. Structure of the auditory system of the weta Hemideina crassidens (Blanchard, 1851) (Orthoptera, Ensifera, Gryllacridoidea, Stenopelmatidae). 1. Morphology and histology. Cell Tissue Res. 1981;217(2):321–43. Bässler U. Sense organs in the femur of the stick insect and their relevance to the control of position of the femur-tibia-joint. J Comp Physiol. 1977;121(1):99–113. Bässler U. Neural basis of elementary behaviour of stick insects. Berlin: Springer; 1983. Barker AJ. Brains and speciation: Control of behavior. Curr Opin Neurobiol. 2021;71:158–163. Bässler U. The femur-tibia control system of stick insects: a model system for the study of the neural basis of joint control. Brain Res Rev. 1993;18(2):207–26. Bradler S, Buckley TR. Biodiversity of Phasmatodea. In: Foottit RG, Adler PH, editors. Insect biodiversity: science and society, Vol. II. Hoboken, NJ: Wiley-Blackwell; 2018. p. 281–313. Büscher TH, Buckley TR, Grohmann C, Gorb SN, Bradler S. The evolution of tarsal adhesive microstructures in stick and leaf insects (Phasmatodea). Front Ecol Evol. 2018;6:69. Büschges A, Gruhn M. Mechanosensory feedback in walking: from joint control to locomotor patterns. Adv Insect Physiol. 2008;34:193–230. Čokl A, Virant-Doberlet M, Zorović M. Sense organs involved in the vibratory communication of bugs. In: Drosopoulos S, Claridge MF, editors. Insect sounds and communication: physiology, behaviour, ecology and evolution. Boca Raton, FL: CRC Press; 2006. p. 71–80. Dambach M. Der vibrationssinn der Grillen. J Comp Physiol. 1972;79(3):281–304. Debaisieux P. Organes scolopidiaux des pattes d’insectes II. Cellule. 1938;47:77–202. Dickerson BH, Fox JL, Sponberg S. Functional diversity from generic encoding in insect campaniform sensilla. Curr Opin Physiol. 2021;19:194–203. Dumont JPC, Robertson RM. Neuronal circuits: an evolutionary perspective. Science. 1986;233(4766):849–53. Eberhard M, Lang D, Metscher B, Pass G, Picker M, Wolf H. Structure and sensory physiology of the leg scolopidial organs in Mantophasmatodea and their role in vibrational communication. Arthropod Struct Dev. 2010;39(4):230–41. Eisner T, Morgan RC, Attygalle AB, Smedley SR, Herath KB, Meinwald J. Defensive production of quinoline by a phasmid insect (Oreophoetes peruana). J Exp Biol. 1997;200:2493–500. Field LH, Matheson T. Chordotonal organs of insects. Adv Insect Physiol. 1998;27:1–228. Friedrich H. Vergleichende Untersuchungen über die tibialen Scolopalorgane einiger Orthopteren. Z wiss Zool. 1929;134:84–148. Godden DH. The motor innervation of the leg musculature and motor output during thanatosis in the stick insect Carausius morosus. Br J Comp Physiol. 1972;80(2):201–25. Goldammer J, Büschges A, Schmidt J. Motoneurons, DUM cells, and sensory neurons in an insect thoracic ganglion: a tracing study in the stick insect Carausius morosus. J Comp Neurol. 2012;520(2):230–57. Kalmring K, Rössler W, Unrast C. Complex tibial organs in the forelegs, midlegs, and hindlegs of the bushcricketGampsocleis gratiosa (tettigoniidae): comparison of the physiology of the organs. J Exp Zool. 1994;270(2):155–61. Katz PS. Neural mechanisms underlying the evolvability of behaviour. Philos Trans R Soc Lond B Biol Sci. 2011;366(1574):2086–99. Keil TA. Functional morphology of insect mechanoreceptors. Microsc Res Tech. 1997;39(6):506–31. Keshishian H, Bentley D. Embryogenesis of peripheral nerve pathways in grasshopper legs. II. The major nerve routes. Dev Biol. 1983;96(1):103–15. King DG. Evolutionary loss of a neural pathway from the nervous system of a fly (Glossina morsitans/Diptera). J Morphol. 1983;175(1):27–32. Kutsch W, Breidbach O. Homologous structures in the nervous systems of arthropoda. Adv Insect Physiol. 1994;24:1–113. Lakes R, Mücke A. Regeneration of the foreleg tibia and tarsi of Ephippiger ephippiger (Orthoptera: tettigoniidae). J Exp Zool. 1989;250(2):176–87. Lakes-Harlan R, Pollack GS. Pathfinding of peripheral neurons in the central nervous system of an embryonic grasshopper (Chorthippus biguttulus). Cell Tissue Res. 1993;273(1):97–106. Liang X, Sun L, Liu Z. Mechanosensory transduction in Drosophila Melanogaster. Singapore: Springer; 2017. Lin Y, Rössler W, Kalmring K. Morphology of the tibial organs of acrididae: comparison of subgenual and distal organs in fore-, mid-, and hindlegs of Schistocerca gregaria (Acrididae, Catantopinae) and Locusta migratoria (Acrididae, Oedipodinae). J Morphol. 1995;226(3):351–60. Marquardt F. Beiträge zur Anatomie der Muskulatur und der peripheren Nerven von Carausius (Dixippus) morosus. Br Zool Jb Anat Ontogenie Tiere. 1940;66:63–128. Meier T, Reichert H. Developmental mechanisms, homology and evolution of the insect peripheral nervous system. In: Breidbach O, Kutsch W, editors. The nervous systems of invertebrates: an evolutionary and comparative approach. Basel: Birkhäuser; 1995. p. 249–71. Michel K. Das Tympanalorgan von Gryllus bimaculatus Degeer (Saltatoria, Gryllidae). Z Morph Tiere. 1974;77(4):285–315. Mücke A. Innervation pattern and sensory supply of the midleg of Schistocerca gregaria (Insecta, Orthopteroidea). Zoomorphology. 1991;110(4):175–87. Pitman RM, Tweedle CD, Cohen MJ. The form of nerve cells: determination by cobalt impregnation. In: Nicholson C, Kater SB, editors. Intracellular staining in neurobiology. Berlin: Springer; 1973. p. 83–97. Pringle JWS. Proprioception in insects. J Exp Biol. 1938;15(1):114–31. Riedl R. Order in living organisms. A systems analysis of evolution. Chichester: John Wiley and Sons; 1978. Rössler W, Hübschen A, Schul J, Kalmring K. Functional morphology pof bushcricket ears: comparison between two species belonging tot he Phaneropterinae and Decticina (Insecta, Ensifera). Zoomorphology. 1994;114(1):39–46. Sanchez D, Ganfornina MD, Bastiani MJ. Contributions of an orthopteran to the understanding of neuronal pathfinding. Immunol Cell Biol. 1995;73:565–74. Schnorbus H. Die subgenualen Sinnesorgane von Periplaneta americana: Histologie und Vibrationsschwellen. Z Vergl Physiol. 1971;71(1):14–48. Schumacher R. Morphologische untersuchungen der tibialen tympanalorgane von neun einheimischen laubheuschrecken-arten (Orthoptera, Tettigonioidea). Z Morph Tiere. 1973;75(4):267–82. Schwenk K, Wagner GP. Constraint. In: Hall BK, Olson WM, editors. Keywords and concepts in evolutionary developmental biology. Cambridge, MA: Harvard University Press; 2003. p. 52–61. Sellick JT. The micropylar plate of the eggs of Phasmida, with a survey of the range of plate form within the order. Syst Entomol. 1998;23(3):203–28. Shaw SR. Detection of airborne sound by a cockroach “vibration detector”: a possible missing link in insect auditory evolution. J Exp Biol. 1994;193(1):13–47. Simon S, Letsch H, Bank S, Buckley TR, Donath A, Liu S, et al. Old world and new world phasmatodea: phylogenomics resolve the evolutionary history of stick and leaf insects. Front Ecol Evol. 2019;7:345. Strausfeld NJ. Variations and invariants of cell arrangements in the nervous system of insects. (A review of neuronal arrangements in the visual system and corpora pedunculata). Verh Dt Zool Ges. 1970;64:97–108. Strauß J. The scolopidial accessory organs and Nebenorgans in orthopteroid insects: comparative neuroanatomy, mechanosensory function, and evolutionary origin. Arthropod Struct Dev. 2017;46(6):765–76. Strauß J. Neuronal innervation of the subgenual organ complex and the tibial campaniform sensilla in the stick insect midleg. Insects. 2020; 11(1):40. Strauß J, Lakes-Harlan R. Sensory neuroanatomy of stick insects highlights the evolutionary diversity of the orthopteroid subgenual organ complex. J Comp Neurol. 2013;521(16):3791–803. Strauß J, Lakes-Harlan R. Vibrational sensitivity of the subgenual organ complex in female Sipyloidea sipylus stick insects in different experimental paradigms of stimulus direction, leg attachment, and ablation of a connective tibial sense organ. Comp Biochem Physiol A. 2017;203:100–8. Strauß J, Lomas K, Field LH. The complex tibial organ of the New Zealand ground weta: sensory adaptations for vibrational signal detection. Sci Rep. 2017;7(1):2031. Strauß J, Moritz L, Rühr PT. The subgenual organ complex in stick insects: Functional morphology and mechanical coupling of a complex mechanosensory organ. Front Ecol Evol. 2021a;9:632493. Strauß J, Riesterer AS, Lakes-Harlan R. How many mechanosensory organs in the bushcricket leg? Neuroanatomy of the scolopidial accessory organ in Tettigoniidae (Insecta: Orthoptera). Arthropod Struct Dev. 2016;45(1):31–41. Strauß J, Stritih N. The accessory organ, a scolopidial sensory organ, in the cave cricket Troglophilus neglectus (Orthoptera: Ensifera: Rhaphidophoridae). Acta Zool. 2016;97:187–95. Strauß J, Stritih N. Neuronal regression of internal leg vibroreceptor organs in a cave-dwelling insect (Orthoptera: Rhaphidophoridae: Dolichopoda araneiformis). Brain Behav Evol. 2017;89(2):104–16. Strauß J, Stritih N, Lakes-Harlan R. The subgenual organ complex in the cave cricket Troglophilus neglectus (Orthoptera: Rhaphidophoridae): comparative innervation and sensory evolution. Roy Soc Open Sci. 2014;1(2):140240. Strauß J, Stritih-Peljhan N, Nieri R, Virant-Doberlet M, Mazzoni V. Communication by substrate-borne mechanical waves in insects: from basic to applied biotremology. Adv Insect Physiol. 2021b;61:189–307. Tosches MA. Developmental and genetic mechanisms of neural circuit evolution. Dev Biol. 2017;431(1):16–25. Yager DD. Structure, development, and evolution of insect auditory systems. Microsc Res Tech. 1999;47(6):380–400. Zill SN, Büschges A, Schmitz J. Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, Carausius morosus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2011;197(8):851–67. Zill S, Schmitz J, Büschges A. Load sensing and control of posture and locomotion. Arthropod Struct Dev. 2004;33(3):273–86. Article / Publication Details

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Abstract of Original Paper

Received: January 14, 2022
Accepted: May 19, 2022
Published online: June 02, 2022

Number of Print Pages: 10
Number of Figures: 5
Number of Tables: 0

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

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