The scolopidial accessory organs and Nebenorgans in orthopteroid insects: Comparative neuroanatomy, mechanosensory function, and evolutionary origin

Autrum, 1960, Phasische und tonische Antworten vom Tympanalorgan von Tettigonia viridissima, Acustica, 10, 339 Ball, 1981, Structure of the auditory system of the weta Hemideina crassidens (Blanchard, 1851) (Orthoptera, Ensifera, Gryllacridoidea, Stenopelmatidae). 1. Morphology and Histology, Cell Tissue Res., 217, 321, 10.1007/BF00233584 Büschges, 1994, The physiology of sensory cells in the ventral scoloparium of the stick insect femoral chordotonal organ, J. Exp. Biol., 189, 285, 10.1242/jeb.189.1.285 Burns, 1974, Structure and physiology of the locust femoral chordotonal organ, J. Insect Physiol., 20, 1319, 10.1016/0022-1910(74)90236-4 Čokl, 1995, Physiology of atympanate tibial organs in forelegs and midlegs of the cave-living Ensifera, Troglophilus neglectus (Raphidophoridae, Gryllacridoidea), J. Exp. Zool., 273, 376, 10.1002/jez.1402730503 Comer, 2011, Active touch in orthopteroid insects: behaviours, multisensory substrates and evolution, Phil Trans. R. Soc. Lond B, 366, 3006, 10.1098/rstb.2011.0149 Debaisieux, 1938, Organes scolopidiaux des pattes d’insectes II, Cellule, 47, 77 Eberhard, 2010, Structure and sensory physiology of the leg scolopidial organs in Mantophasmatodea and their role in vibrational communication, Arthropod Struct. Dev., 39, 230, 10.1016/j.asd.2010.02.002 Eibl, 1978, Morphology of the sense organs in the proximal parts of the tibiae of Gryllus campestris L. and Gryllus bimaculatus deGeer Insecta, Ensifera, Zoomorphologie, 89, 185, 10.1007/BF00993947 Field, 2001, Sensory physiology, 429 Field, 1998, Chordotonal organs in insects, Adv. Insect Physiol., 27, 1, 10.1016/S0065-2806(08)60013-2 Field, 1989, The femoral chordotonal organ: a bifunctional orthopteran (Locusta migratoria) sense organ?, Comp. Biochem. Physiol. A, 93, 729, 10.1016/0300-9629(89)90494-5 Friedrich, 1929, Vergleichende Untersuchungen über die tibialen Scolopalorgane einiger Orthopteren, Z. wiss. Zool., 134, 84 Friedrich, 1930, Weitere vergleichende Untersuchungen über die tibialen Scolopalorgane bei Orthopteren, Z. wiss. Zool., 137, 30 Fullard, 1994, Auditory changes in noctuid moths endemic to a bat-free habitat, J. Evol. Biol., 7, 435, 10.1046/j.1420-9101.1994.7040435.x Fullard, 1998, The sensory coevolution of moths and bats, 279 Fullard, 2007, Neural evolution in the bat-free habitat of Tahiti: partial regression in an anti-predator auditory system, Biol. Lett., 22, 26, 10.1098/rsbl.2006.0550 Fullard, 2010, Release from bats: genetic distance and sensoribehavioural regression in the Pacifi field cricket, Teleogryllus oceanicus, Naturwissenschaften, 97, 53, 10.1007/s00114-009-0610-1 Füller, 1973, Die Ultrastruktur der femoralen Chordotonalorgane von Carausius morosus Br, Zool. Jb Anat., 91, 574 Göpfert, 2016, Hearing in insects, Annu. Rev. Entomol., 61, 257, 10.1146/annurev-ento-010715-023631 Grosch, 1985, Vibration receptors of larvae and of imagines in locusts: location on the leg, central projection and physiology, 151 Haas, 2016 Hedwig, 2001, Singing and hearing: neuronal mechanisms of acoustic communication in Orthopterans, Zoology, 103, 140 Heller, 2016, Fauna Europeae – Orthopteroid orders, Biodivers. Data J., 4, e8905, 10.3897/BDJ.4.e8905 von Helversen, 1987, Innate receiver mechanisms in the acoustic communication of orthopteran insects, 104 Houtermans, 1974, Zur Morphologie der atympanalen tibialen Scolopalorgane von Tettigonia viridissima L. (Orthoptera, Tettigoniidae), Z Morphol. Tiere, 78, 281, 10.1007/BF00635999 Howse, 1965, The structure of the subgenual organ and certain other mechanoreceptors of the termite Zootermopsis angusticollis (Hagen), Proc. R. Ent Soc. Lond A, 40, 137 Howse, 1968, The fine structure and functional organization of chordotonal organs, Symp. Zool. Soc. Lond, 23, 167 Huber, 1983, Neural correlates of Orthopteran and Cicada phonotaxis, 108 Huber, 1990, Cricket neuroethology: neuronal basis of intraspecific acoustic communication, Adv. Study Behav., 19, 299, 10.1016/S0065-3454(08)60206-5 Hummel, 2016, Gating of acoustic transducer channels is shaped by biomechanical filter processes, J. Neurosci., 36, 2377, 10.1523/JNEUROSCI.3948-15.2016 Hustert, 1981, Distribution and specific central projections of mechanoreceptors in the thorax and proximal leg joints of locusts. III. The external mechanoreceptors: the campaniform sensilla, Cell Tissue Res., 216, 97, 10.1007/BF00234547 Hutchings, 1983, Insect sound and vibration receptors, 181 Kalmring, 1985, Vibrational communication in insects (reception and integration of vibratory information), 127 Kalmring, 1994, Complex tibial organs in the forelegs, midlegs, and hindlegs of the bushcricket Gampsocleis gratiosa (Tettigoniidae): comparison of the physiology of the organs, J. Exp. Zool., 270, 155, 10.1002/jez.1402700205 Kavlie, 2013, Chordotonal organs, Curr. Biol., 23, R334, 10.1016/j.cub.2013.03.048 Keil, 1998, The structure of integument al mechanoreceptors, vol. 11, 385 Keil, 2012, Sensory cilia in arthropods, Arthropod Struct. Dev., 41, 515, 10.1016/j.asd.2012.07.001 Keshishian, 1983, Embryogenesis of peripheral nerve pathways in grasshopper legs. I. The initial nerve pathway tot he CNS, Dev. Biol., 96, 89, 10.1016/0012-1606(83)90314-7 Keshishian, 1983, Embryogenesis of peripheral nerve pathways in grasshopper legs. II. The major nerve routes, Dev. Biol., 96, 103, 10.1016/0012-1606(83)90315-9 Kittmann, 1992, Functional specialisation of the scoloparia of the femoral chordotonal organ in stick insects, J. Exp. Biol., 173, 91, 10.1242/jeb.173.1.91 Knetsch, 1939, Die Korrelation der Ausbildung der Tympanalorgane, der Flügel, der Stridulationsapparate und anderer Organsysteme bei den Orthopteren, Arch. Naturgesch, 8, 1 Kühne, 1982, Neurophysiology of the vibration sense in locusts and bushcrickets: response characteristics of single receptor units, J. Insect Physiol., 28, 155, 10.1016/0022-1910(82)90123-8 Kutsch, 1994, Homologous structures in the nervous system of Arthropoda, Adv. Insect Physiol., 24, 1, 10.1016/S0065-2806(08)60082-X Lakes, 1990, Neuroanatomy of tettigoniids, 166 Lakes-Harlan, 1991, The auditory system of an atympanate bushcricket Phasmodes ranatriformes (Westwood) (Tettigoniidae: Orthoptera), J. Exp. Biol., 158, 307, 10.1242/jeb.158.1.307 Lehmann, 2010, The auditory system of non-calling grasshoppers (Melanoplinae: Podismini) and the evolutionary regression of their tympanal ears, J. Comp. Physiol. A, 196, 807, 10.1007/s00359-010-0560-2 Lewis, 1974, The physiology of the tettigoniid ear. I. The implications of the anatomy of the ear to its function in sound reception, J. Exp. Biol., 60, 821, 10.1242/jeb.60.3.821 Lin, 1995, Morphology of the tibial organs of Acrididae: comparison of subgenual and distal organs in fore-, mid-, and hindlegs of Schistocerca gregaria (Acrididae, Catantopidae) and Locusta migratoria (Acrididae, Oedipodinae), J. Morphol., 226, 351, 10.1002/jmor.1052260310 Matheson, 1990, Innervation of the metathoracic femoral chordotonal organ of Locusta migratoria, Cell Tissue Res., 259, 551, 10.1007/BF01740783 McIver, 1985, Mechanoreception, 71 Meier, 1990, Embryonic development and evolutionary origin of the Orthopteran auditory organs, J. Neurobiol., 21, 592, 10.1002/neu.480210407 Michel, 1974, Das Tympanalorgan von Gryllus bimaculatus deGeer (Saltatoria, Gryllidae), Z Morphol. Tiere, 77, 285, 10.1007/BF00298805 Michel, 1979, Ein neuer Typ eines Grillenohrs: Konstruktion und Ultrastruktur des Tympanalorgans von Cycloptiloides canariensis (Bolivar) (Mogoplistinae, Gryllidae), Zool. Anz, 203, 139 Michel, 1980, Die Scolopalorgane in den atympanalen Tibien von Gryllus bimaculatus De Geer und Phaeophilacris spectrum Saussure (Gryllidae, Insecta), Zool. Jb Anat. Ontog. Tiere, 103, 122 Misof, 2014, Phylogenomics resolves the timing and pattern of insect evolution, Science, 346, 763, 10.1126/science.1257570 Montealegre-Z, 2015, Biomechanics of hearing in katydids, J. Comp. Physiol. A, 201, 5, 10.1007/s00359-014-0976-1 Moran, 1975, The fine structure of the cockroach subgenual organ, Tissue Cell, 7, 91, 10.1016/S0040-8166(75)80009-7 Mücke, 1991, Innervation pattern and sensory supply of the midleg of Schistocerca gregaria (Insecta, Orthopteroidea), Zoomorphology, 110, 175, 10.1007/BF01633002 Nijenhuis, 1952, A micro-morphological study on the sensory supply of the mesothoracic leg of the American cockroach, Periplaneta americana, Proc. Kon. Ned. Akad. Wet. Ser. C, 55, 300 Nishino, 2003, Somatotopic mapping of chordotonal organ neurons in a primitive ensiferan, the New Zealand tree weta Hemideina femorata: I. Femoral chordotonal organ, J. Comp. Neurol., 464, 312, 10.1002/cne.10779 Nishino, 1997, Three neural groups in the femoral chordotonal organ of the cricket Gryllus bimaculatus: central projections and soma arrangement and displacement during joint flexion, J. Exp. Biol., 200, 2583, 10.1242/jeb.200.20.2583 Nishino, 2003, Somatotopic mapping of chordotonal organ neurons in a primitive ensiferan, the New Zealand tree weta Hemideina femorata: II. Complex tibial organ, J. Comp. Neurol., 464, 327, 10.1002/cne.10780 Nishino, 2016, Chordotonal organs in hemipteran insects: unique peripheral structures but conserved central organization revealed by comparative neuroanatomy, Cell Tissue Res., 366, 549, 10.1007/s00441-016-2480-0 Nocke, 1975, Physical and physiological properties of the tettigoniid (‘grasshopper’) ear, J. Comp. Physiol., 100, 25, 10.1007/BF00623929 Oldfield, 1982, Tonotopic organisation of auditory receptors in Tettigoniidae (Orthoptera: Ensifera), J. Comp. Physiol. A, 147, 461, 10.1007/BF00612011 Oldfield, 1984, Physiology of auditory receptors in two species of Tettigoniidae (Orthoptera: Ensifera). Alternative tonotopic organisations of the auditory organ, J. Comp. Physiol. A, 155, 689, 10.1007/BF00610855 Pflüger, 1988, The organization of mechanosensory neuropiles in locust thoracic ganglia, Philos. Trans. R. Soc. Lond B, 321, 1, 10.1098/rstb.1988.0090 Pollack, 2016 Pumphrey, 1940, Hearing in insects, Biol. Rev., 15, 107, 10.1111/j.1469-185X.1940.tb00944.x Ridgel, 2000, Encoding of forces by cockroach tibial campaniform sensilla: implications in dynamic control of posture and locomotion, J. Comp. Physiol. A, 186, 359, 10.1007/s003590050436 Robinson, 2002, Sound signalling in orthoptera, Adv. Insect Phys., 29, 151, 10.1016/S0065-2806(02)29003-7 Römer, 1983, Tonotopic organisation of the auditory neuropile in the bushcricket, Tettigonia viridissima, Nature, 306, 60, 10.1038/306060a0 Römer, 1988, Organization of a sensory neuropile in the auditory pathway of two groups of Orthoptera, J. Comp. Neurol., 275, 201, 10.1002/cne.902750204 Römer, 2010, The signaller's dilemma: a cost–benefit analysis of public and private communication, PLoS One, 5, 10.1371/journal.pone.0013325 Schildberger, 1989, Central auditory pathway: neuronal correlates of phonotactic behaviour, 423 Schmitz, 1991, Central projections of leg sense organs in Carausius morosus (Insecta, Phasmida), Zoomorphology, 111, 19, 10.1007/BF01632707 Schnorbus, 1971, Die subgenualen Sinnesorgane von Periplaneta americana: Histologie und Vibrationsschwellen, Z Vergl Physiol., 71, 14, 10.1007/BF03395969 Schumacher, 1973, Morphologische Untersuchungen der tibialen Tympanalorgane von neun einheimischen Laubheuschrecken-Arten (Orthoptera, Tettigonioidea), Z Morph Tiere, 75, 267, 10.1007/BF00288474 Schumacher, 1975, The crista acustica of the Tettigonioidea (Orthoptera), Z Naturforschung C, 30, 552 Schumacher, 1975, Scanning-electrone-microscopy description of the tibial tympanal organ of the Tettigonioidea (Orthoptera, Ensifera), Z Morphol. Tiere, 81, 209, 10.1007/BF00278370 Schumacher, 1975, Vergleich des primären Rezeptorbereichs der tympanalen und atympanalen tibialen Skolopalorgane von 14 mitteleuropäischen Laubheuschrecken-Arten (Orthoptera: Tettigonioidea), Entomol. Ger., 1, 97 Schumacher, 1979, Zur funktionellen Morphologie des auditiven Systems der Laubheuschrecken (Orthoptera: Tettigonioidea), Entomol. Gen., 5, 321, 10.1127/entom.gen/5/1979/321 Schwabe, 1906, Beiträge zur Morphologie und Histologie der tympanalen Sinnesapparate der Orthopteren, Zoologica, 50, 1 Shaw, 1994, Detection of airborne sound by a cockroach ‘‘vibration detector’’: a possible missing link in insect auditory evolution, J. Exp. Biol., 193, 13, 10.1242/jeb.193.1.13 Song, 2015, 300 million years of diversification: elucidating the patterns of orthopteran evolution based on comprehensive taxon and gene sampling, Cladistics, 31, 621, 10.1111/cla.12116 Strauß, 2017, The scolopidial accessory organ in the Jerusalem cricket (Orthoptera: Stenopelmatidae), Arthropod. Struct. Dev., 46, 171, 10.1016/j.asd.2016.12.001 Strauß, 2008, Neuroanatomy and physiology of the complex tibial organ of an atympanate ensiferan, Ametrus tibialis (Brunner von Wattenwyl, 1888) (Gryllacrididae, Orthoptera) and evolutionary implications, Brain Behav. Evol., 71, 167, 10.1159/000114405 Strauß, 2010, Neuroanatomy of the complex tibial organ in the splay- footed Comicus calcaris Irish 1986 (Orthoptera: Ensifera: Schizodactylidae), J. Comp. Neurol., 518, 4567, 10.1002/cne.22478 Strauß, 2013, Sensory neuroanatomy of stick insects highlights the evolutionary diversity of the orthopteroid subgenual organ complex, J. Comp. Neurol., 521, 3791, 10.1002/cne.23378 Strauß, 2014, Sensory evolution of hearing in tettigoniids with differing communication systems, J. Evol. Biol., 27, 200, 10.1111/jeb.12294 Strauß, 2017, The complex tibial organ of the New Zealand ground weta: sensory adaptations for vibrational signal detection, Sci. Rep., 7, 2031, 10.1038/s41598-017-02132-1 Strauß, 2016, How many mechanosensory organs in the bushcricket leg? Neuroanatomy of the scolopidial accessory organ in Tettigoniidae (Insecta: Orthoptera), Arthropod Struct. Dev., 45, 31, 10.1016/j.asd.2015.11.002 Strauß, 2016, The accessory organ, a scolopidial sensory organ, in the cave cricket Troglophilus neglectus (Orthoptera: Ensifera: Rhaphidophoridae), Acta Zool. (Stockholm), 97, 187, 10.1111/azo.12116 Strauß, 2017, Neuronal regression of internal leg vibroreceptor organs in a cave- dwelling insect (Orthoptera: Rhaphidophoridae: Dolichopoda araneiformis), Brain Behav. Evol., 89, 104, 10.1159/000462957 Strauß, 2014, The subgenual organ complex in the cave cricket Troglophilus neglectus (Orthoptera: Rhaphidophoridae): comparative innervation and sensory evolution, R. Soc. Open Sci., 1 Strauß, 2015, Selective forces on origin, adaptation and reduction of tympanal ears in insects, J. Comp. Physiol. A, 201, 155, 10.1007/s00359-014-0962-7 Stumpner, 1996, Tonotopic organization of the hearing organ in a bushcricket, Naturwissenschaften, 83, 81 Theophilidis, 1986, The femoral chordotonal organ of Decticus albifrons (Orthoptera: Tettigoniidae). I. Structure, Comp. Biochem. Physiol. A, 84, 529, 10.1016/0300-9629(86)90361-0 van Staaden, 1998, Evolutionary transition from stretch to hearing in ancient grasshoppers, Nature, 394, 773, 10.1038/29517 Yack, 2004, The structure and function of auditory chordotonal organs in insects, Microsc. Res. Tech., 63, 315, 10.1002/jemt.20051 Young, 1974, Structure and development of the auditory system in the prothoracic leg of the cricket Teleogryllus commodus (Walker) I. Adult structure, Z Zellforsch Mikrosk Anat., 147, 293, 10.1007/BF00307466 Zhantiev, 1978, Morphofunctional organization of tympanal organs in Tettigonia cantans (Orthoptera, Tettigoniidae), Zool. Zh, 57, 1012 Zill, 2011, Encoding of force increases and decreases by tibial campaniform sensilla in the stick insect, Carausius morosus, J. Comp. Physiol. A, 197, 851, 10.1007/s00359-011-0647-4