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Abstract

Insect hearing has independently evolved multiple times in the context of intraspecific communication and predator detection by transforming proprioceptive organs into ears. Research over the past decade, ranging from the biophysics of sound reception to molecular aspects of auditory transduction to the neuronal mechanisms of auditory signal processing, has greatly advanced our understanding of how insects hear. Apart from evolutionary innovations that seem unique to insect hearing, parallels between insect and vertebrate auditory systems have been uncovered, and the auditory sensory cells of insects and vertebrates turned out to be evolutionarily related. This review summarizes our current understanding of insect hearing. It also discusses recent advances in insect auditory research, which have put forward insect auditory systems for studying biological aspects that extend beyond hearing, such as cilium function, neuronal signal computation, and sensory system evolution.

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2016-03-11
2024-03-28
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Literature Cited

  1. Albert JT, Nadrowski B, Göpfert MC. 1.  2007. Mechanical signatures of transducer gating in the Drosophila ear. Curr. Biol. 17:1000–6 [Google Scholar]
  2. Bechstedt S, Albert JT, Kreil DP, Müller-Reichert T, Göpfert MC, Howard J. 2.  2010. A doublecortin containing microtubule-associated protein is implicated in mechanotransduction in Drosophila sensory cilia. Nat. Commun. 1:11 [Google Scholar]
  3. Bechstedt S, Howard J. 3.  2007. Models of hair cell mechanotransduction. Curr. Top. Membr. 59:399–424 [Google Scholar]
  4. Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N. 4.  et al. 1999. Math1: an essential gene for the generation of inner ear hair cells. Science 284:1837–41 [Google Scholar]
  5. Blankers T, Hennig RM, Gray DA. 5.  2015. Conservation of multivariate female preference functions and preference mechanisms in three species of trilling field crickets. J. Evol. Biol. 28:630–41 [Google Scholar]
  6. Boo KS, Richards AG. 6.  1975. Fine structure of the scolopidia in the Johnston's organ of male Aedes aegypti (L.) (Diptera: Culicidae). Int. J. Insect Morphol. Embryol. 4:549–66 [Google Scholar]
  7. Boyan GS. 7.  1993. Another look at insect audition: the tympanic receptors as an evolutionary specialization of the chordotonal system. J. Insect Physiol. 39:187–200 [Google Scholar]
  8. Boyan GS, Ball EE. 8.  1993. The grasshopper, Drosophila and neuronal homology (advantages of the insect nervous system for the neuroscientist). Prog. Neurobiol. 41:657–82 [Google Scholar]
  9. Cator LJ, Arthur BJ, Harrington LC, Hoy RR. 9.  2009. Harmonic convergence in the love songs of the dengue vector mosquito. Science 323:1077–79 [Google Scholar]
  10. Cheng LE, Song W, Looger LL, Jan LY, Jan YN. 10.  2010. The role of the TRP channel NompC in Drosophila larval and adult locomotion. Neuron 67:373–80 [Google Scholar]
  11. Chung YD, Zhu J, Han Y, Kernan MJ. 11.  nompA encodes a PNS-specific ZP domain protein required to connect mechanosensory dendrites. Neuron 29:415–28 [Google Scholar]
  12. Clemens J, Hennig RM. 12.  2013. Computational principles underlying the recognition of acoustic signals in insects. J. Comp. Neurosci. 35:75–85 [Google Scholar]
  13. Clemens J, Kutzki O, Ronacher B, Schreiber S, Wohlgemuth S. 13.  2011. Efficient transformation of an auditory population code in a “small” sensory system. PNAS 108:13812–17 [Google Scholar]
  14. Cocroft RB. 14.  2011. The public world of insect vibrational communication. Mol. Ecol. 20:2041–43 [Google Scholar]
  15. Conner WE, Corcoran AJ. 15.  2012. Sound strategies: the 65-million-year-old battle between bats and insects. Annu. Rev. Entomol. 57:21–39 [Google Scholar]
  16. Cosetti M, Kulang D, Kotla S, O'Brien P, Eberl DF, Hannan F. 16.  2008. Unique transgenic animal model for hereditary hearing loss. Ann. Otol. Rhinol. Laryngol. 117:827–33 [Google Scholar]
  17. Creutzig F, Wohlgemuth S, Stumpner A, Benda J, Ronacher B, Herz AV. 17.  2009. Timescale-invariant representation of acoustic communication signals by a bursting neuron. J. Neurosci. 29:2575–80 [Google Scholar]
  18. Dobler S, Heller K-G, von Helversen O. 18.  1994. Song pattern recognition and an auditory time window in the female bush-cricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J. Comp. Physiol. A 175:67–74 [Google Scholar]
  19. Dong PD, Todi SV, Eberl DF, Boekhoff-Falk G. 19.  2003. Drosophila spalt/spalt-related mutants exhibit Townes–Brocks' syndrome phenotypes. PNAS 100:10293–98 [Google Scholar]
  20. Doolan JM, Young D. 20.  1981. The organization of the auditory organ of the bladder cicada, Cystosoma saundersii. Philos. Trans. R. Soc. B 291:525–40 [Google Scholar]
  21. Eberl DF. 21.  1999. Feeling the vibes: chordotonal mechanisms in insect hearing. Curr. Opin. Neurobiol. 9:389–93 [Google Scholar]
  22. Effertz T, Nadrowski B, Piepenbrock D, Albert JT, Göpfert MC. 22.  2012. Direct gating and mechanical integrity of Drosophila auditory transducers require TRPN1. Nat. Neurosci. 15:1198–200 [Google Scholar]
  23. Effertz T, Wiek R, Göpfert MC. 23.  2011. NOMPC TRP channel is essential for Drosophila sound receptor function. Curr. Biol. 21:592–97 [Google Scholar]
  24. Fettiplace R, Fuchs PA. 24.  1999. Mechanisms of hair cell tuning. Annu. Rev. Physiol. 61:809–34 [Google Scholar]
  25. Field LH, Matheson T. 25.  1998. Chordotonal organs of insects. Adv. Insect Physiol. 27:1–228 [Google Scholar]
  26. Forrest TG, Read MP, Farris HE, Hoy RR. 26.  1997. A tympanal hearing organ in scarab beetles. J. Exp. Biol. 200:601–6 [Google Scholar]
  27. Fritzsch B, Eberl DF, Beisel KW. 27.  2010. The role of bHLH genes in ear development and evolution: revisiting a 10-year-old hypothesis. Cell. Mol. Life Sci. 67:3089–99 [Google Scholar]
  28. Fritzsch B, Straka H. 28.  2014. Evolution of vertebrate mechanosensory hair cells and inner ears: toward identifying stimuli that select mutation driven altered morphologies. J. Comp. Physiol. A 200:5–18 [Google Scholar]
  29. Fullard JH. 29.  2006. Evolution of hearing in moths: the ears of Oenosandra boisduvalii (Noctuoidea: Oenosandridae). Aust. J. Zool. 54:51–56 [Google Scholar]
  30. Fullard JH, Dawson JW, Jacobs DS. 30.  2003. Auditory encoding during the last moment of a moth's life. J. Exp. Biol. 206:281–94 [Google Scholar]
  31. Fullard JH, Yack JE. 31.  1993. The evolutionary biology of insect hearing. Trends Ecol. Evol. 8:248–52 [Google Scholar]
  32. Geurten BR, Spalthof C, Göpfert MC. 32.  2013. Insect hearing: active amplification in tympanal ears. Curr. Biol. 23:R950–52 [Google Scholar]
  33. Gold JI, Shadlen MN. 33.  2007. The neural basis of decision making. Annu. Rev. Neurosci. 30:535–47 [Google Scholar]
  34. Gong Z, Son W, Chung YD, Kim J, Shin DW. 34.  et al. 2004. Two interdependent TRPV channel subunits, Inactive and Nanchung, mediate hearing in Drosophila. J. Neurosci. 24:9059–66 [Google Scholar]
  35. Göpfert MC, Albert JT. 35.  2015. Hearing in Drosophila. Curr. Opin. Neurobiol. 34:79–85 [Google Scholar]
  36. Göpfert MC, Albert JT, Nadrowski B, Kamikouchi A. 36.  2006. Specification of auditory sensitivity by Drosophila TRP channels. Nat. Neurosci. 9:999–1000 [Google Scholar]
  37. Göpfert MC, Humphris AD, Albert JT, Robert D, Hendrich O. 37.  2005. Power gain exhibited by motile mechanosensory neurons in Drosophila ears. PNAS 102:325–30 [Google Scholar]
  38. Göpfert MC, Robert D. 38.  2001. Active auditory mechanics in mosquitoes. Proc. R. Soc. B 258:333–39 [Google Scholar]
  39. Göpfert MC, Robert D. 39.  2002. Motion generation by Drosophila mechanosensory neurons. PNAS 100:5514–19 [Google Scholar]
  40. Göpfert MC, Robert D. 40.  2008. Active processes in insect hearing. Springer Handbook of Auditory Research 30 Active Processes and Otoacoustic Emissions in Hearing GA Manley, RR Fay, AN Popper 191–201 New York: Springer [Google Scholar]
  41. Göpfert MC, Stocker H, Robert D. 41.  2002. atonal is required for exoskeletal joint formation in the Drosophila auditory system. Dev. Dyn. 225:106–9 [Google Scholar]
  42. Göpfert MC, Surlykke A, Wasserthal LT. 42.  2002. Tympanal and atympanal ‘mouth-ears’ in hawkmoths (Sphingidae). Proc. R. Soc. B 259:89–95 [Google Scholar]
  43. Göpfert MC, Wasserthal LT. 43.  1999. Auditory sensory cells in hawkmoths: identification, physiology and structure. J. Exp. Biol. 202:1579–87 [Google Scholar]
  44. Göpfert MC, Wasserthal LT. 44.  1999. Hearing with the mouthparts: behavioural responses and the structural basis of ultrasound perception in acherontiine hawkmoths. J. Exp. Biol. 202:909–18 [Google Scholar]
  45. Grimaldi D, Engel MS. 45.  2005. Evolution of the Insects Cambridge, UK: Cambridge Univ. Press
  46. Gu JJ, Montealegre-Z F, Robert D, Engel MS, Qiao GX, Ren D. 46.  2012. Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females. PNAS 109:3868–73 [Google Scholar]
  47. Hassan BA, Bellen HJ. 47.  2000. Doing the MATH: Is the mouse a good model for fly development?. Genes Dev. 14:1852–65 [Google Scholar]
  48. Hedwig B. 48.  1994. A cephalothoracic command system controls stridulation in the acridid grasshopper Omocestus viridulus L. J. Neurophysiol. 72:2015–25 [Google Scholar]
  49. Hedwig B, Poulet JF. 49.  2004. Complex auditory behaviour emerges from simple reactive steering. Nature 430:781–85 [Google Scholar]
  50. Hennig RM, Franz A, Stumpner A. 50.  2004. Processing of auditory information in insects. Microsc. Res. Tech. 63:351–74 [Google Scholar]
  51. Hennig RM, Heller KG, Clemens J. 51.  2014. Time and timing in the acoustic recognition system of crickets. Front. Physiol. 5:286 [Google Scholar]
  52. Hennig RM, Weber T. 52.  1997. Filtering of temporal parameters of the calling song by cricket females of two closely related species: a behavioral analysis. J. Comp. Physiol. A 180:621–30 [Google Scholar]
  53. Hildebrandt KJ. 53.  2014. Neural maps in insect versus vertebrate auditory systems. Curr. Opin. Neurobiol. 24:82–87 [Google Scholar]
  54. Hildebrandt KJ, Benda J, Hennig RM. 54.  2009. The origin of adaptation in the auditory pathway of locusts is specific to cell type and function. J. Neurosci. 29:2626–36 [Google Scholar]
  55. Hildebrandt KJ, Benda J, Hennig RM. 55.  2011. Multiple arithmetic operations in a single neuron: the recruitment of adaptation processes in the cricket auditory pathway depends on sensory context. J. Neurosci. 31:14142–50 [Google Scholar]
  56. Hildebrandt KJ, Benda J, Hennig RM. 56.  2015. Computational themes of peripheral processing in the auditory pathway of insects. J. Comp. Physiol. A 201:39–50 [Google Scholar]
  57. Holt JR, Pan B, Koussa MA, Asai Y. 57.  2014. TMC function in hair cell transduction. Hear. Res. 311:17–24 [Google Scholar]
  58. Howard J, Bechstedt S. 58.  2004. Hypothesis: A helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors. Curr. Biol. 14:R224–26 [Google Scholar]
  59. Howard J, Hudspeth AJ. 59.  1988. Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cells. Neuron 1:189–99 [Google Scholar]
  60. Hoy RR, Robert D. 60.  1996. Tympanal hearing in insects. Annu. Rev. Entomol. 41:433–50 [Google Scholar]
  61. Hudspeth AJ. 61.  1985. The cellular basis of hearing: the biophysics of hair cells. Science 230:745–52 [Google Scholar]
  62. Hudspeth AJ. 62.  2014. Integrating the active process of hair cells with cochlear function. Nat. Rev. Neurosci. 15:600–14 [Google Scholar]
  63. Jarman AP, Grau Y, Jan LY, Jan YN. 63.  1993. atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73:1307–21 [Google Scholar]
  64. Jarman AP, Groves AK. 64.  2013. The role of Atonal transcription factors in the development of mechanosensitive cells. Semin. Cell Dev. Biol. 24:438–47 [Google Scholar]
  65. Kamikouchi A, Albert JT, Göpfert MC. 65.  2010. Mechanical feedback amplification in Drosophila hearing is independent of synaptic transmission. Eur. J. Neurosci. 31:697–703 [Google Scholar]
  66. Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A. 66.  et al. 2009. The neural basis of Drosophila gravity-sensing and hearing. Nature 458:165–71 [Google Scholar]
  67. Kavlie RG, Fritz JL, Nies F, Göpfert MC, Oliver D. 67.  et al. 2015. Prestin is an anion transporter dispensable for mechanical feedback amplification in Drosophila hearing. J. Comp. Physiol. A 201:51–60 [Google Scholar]
  68. Kavlie RG, Kernan MJ, Eberl DF. 68.  2010. Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility. Genetics 185:177–88 [Google Scholar]
  69. Kennedy HJ, Crawford AC, Fettiplace R. 69.  2005. Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 433:880–83 [Google Scholar]
  70. Kim J, Chung YD, Park DY, Choi S, Shin DW. 70.  et al. 2003. A TRPV family ion channel required for hearing in Drosophila. Nature 424:81–84 [Google Scholar]
  71. Köppl C. 71.  1997. Phase locking to high frequencies in the auditory nerve and cochlear nucleus magnocellularis of the barn owl, Tyto alba. J. Neurosci. 17:3312–21 [Google Scholar]
  72. Kössl M, Möckel D, Weber M, Seyfarth EA. 72.  2008. Otoacoustic emissions from insect ears: evidence of active hearing?. J. Comp. Physiol. A 194:597–609 [Google Scholar]
  73. Kostarakos K, Hedwig B. 73.  2012. Calling song recognition in female crickets: Temporal tuning of identified brain neurons matches behavior. J. Neurosci. 32:9601–12 [Google Scholar]
  74. Kostarakos K, Hedwig B. 74.  2014. Pattern recognition in field crickets: concepts and neural evidence. J. Comp. Physiol. A 201:73–85 [Google Scholar]
  75. Lakes-Harlan R, Lehmann GU. 75.  2015. Parasitoid flies exploiting acoustic communication of insects—comparative aspects of independent functional adaptations. J. Comp. Physiol. A 201:123–32 [Google Scholar]
  76. Langner G, Schreiner CE. 76.  1988. Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J. Neurophysiol. 60:1799–822 [Google Scholar]
  77. Lee E, Sivan-Loukianova E, Eberl DF, Kernan MJ. 77.  2008. An IFT-A protein is required to delimit functionally distinct zones in mechanosensory cilia. Curr. Biol. 18:1899–906 [Google Scholar]
  78. Lee J, Moon S, Cha Y, Chung YD. 78.  2010. Drosophila TRPN(= NOMPC) channel localizes to the distal end of mechanosensory cilia. PLOS ONE 5:e11012 [Google Scholar]
  79. Lehnert BP, Baker AE, Gaudry Q, Chiang AS, Wilson RI. 79.  2013. Distinct roles of TRP channels in auditory transduction and amplification in Drosophila. Neuron 77:115–28 [Google Scholar]
  80. Liang X, Madrid J, Gärtner R, Verbavatz JM, Schiklenk C. 80.  et al. 2013. A NOMPC-dependent membrane-microtubule connector is a candidate for the gating spring in fly mechanoreceptors. Curr. Biol. 23:755–63 [Google Scholar]
  81. Liberman MC. 81.  1978. Auditory-nerve response from cats raised in a low-noise chamber. J. Acoust. Soc. Am. 63:442–45 [Google Scholar]
  82. Machens CK, Schütze H, Franz A, Kolesnikova O, Stemmler MB. 82.  et al. 2003. Single auditory neurons rapidly discriminate conspecific communication signals. Nat. Neurosci. 6:341–42 [Google Scholar]
  83. Martin P, Hudspeth AJ. 83.  2001. Compressive nonlinearity in the hair bundle's active response to mechanical stimulation. PNAS 98:14386–91 [Google Scholar]
  84. Mason AC, Oshinsky ML, Hoy RR. 84.  2001. Hyperacute directional hearing in a microscale auditory system. Nature 410:686–90 [Google Scholar]
  85. Mhatre N. 85.  2015. Active amplification in insect ears: mechanics, models and molecules. J. Comp. Physiol. A 201:19–37 [Google Scholar]
  86. Mhatre N, Robert D. 86.  2013. A tympanal insect ear exploits a critical oscillator for active amplification and tuning. Curr. Biol. 23:1952–57 [Google Scholar]
  87. Michelsen A, Larsen ON. 87.  2008. Pressure difference receiving ears. Bioinspir. Biomim. 3:011001 [Google Scholar]
  88. Miles RN, Su Q, Cui W, Shetye M, Degertekin FL. 88.  et al. 2009. A low-noise differential microphone inspired by the ears of the parasitoid fly Ormia ochracea. J. Acoust. Soc. Am. 125:2013–26 [Google Scholar]
  89. Misof B, Liu S, Meusemann K, Peters RS, Donath A. 89.  et al. 2004. Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–67 [Google Scholar]
  90. Möckel D, Nowotny M, Kössl M. 90.  2014. Mechanical basis of otoacoustic emissions in tympanal hearing organs. J. Comp. Physiol. A 200:681–91 [Google Scholar]
  91. Moir HM, Jackson JC, Windmill JF. 91.  2013. Extremely high frequency sensitivity in a ‘simple’ ear. Biol. Lett. 9:20130241 [Google Scholar]
  92. Montealegre-Z F, Jonsson T, Robson-Brown KA, Postles M, Robert D. 92.  2012. Convergent evolution between insect and mammalian audition. Science 338:968–71 [Google Scholar]
  93. Montealegre-Z F, Robert D. 93.  2015. Biomechanics of hearing in katydids. J. Comp. Physiol. A 201:5–18 [Google Scholar]
  94. Moore DJ, Onoufriadis A, Shoemark A, Simpson MA, zur Lage PI. 94.  et al. 2013. Mutations in ZMYND10, a gene essential for proper axonemal assembly of inner and outer dynein arms in humans and flies, cause primary ciliary dyskinesia. Am. J. Hum. Genet. 93:346–56 [Google Scholar]
  95. Morley EL, Mason AC. 95.  2015. Active auditory mechanics in female black-horned tree crickets (Oecanthus nigricornis). J. Comp. Physiol. A 201:1147–55 [Google Scholar]
  96. Müller P, Robert D. 96.  2001. A shot in the dark: the silent quest of a free-flying phonotactic fly. J. Exp. Biol. 204:1039–52 [Google Scholar]
  97. Nadrowski B, Albert JT, Göpfert MC. 97.  2008. Transducer-based force generation explains active process in Drosophila hearing. Curr. Biol. 18:1365–72 [Google Scholar]
  98. Nadrowski B, Effertz T, Senthilan PR, Göpfert MC. 98.  2011. Antennal hearing in insects: new findings, new questions. Hear. Res. 273:7–13 [Google Scholar]
  99. Nadrowski B, Göpfert MC. 99.  2009. Modeling auditory transducer dynamics. Curr. Opin. Otolaryngol. Head Neck Surg. 17:400–6 [Google Scholar]
  100. Nakano R, Takanashi T, Surlykke A. 100.  2015. Moth hearing and sound communication. J. Comp. Physiol. A 201:111–21 [Google Scholar]
  101. Nesterov A, Spalthoff C, Kandasamy R, Katana R, Rankl NB. 101.  et al. 2015. TRP channels in insect stretch receptors as insecticide targets. Neuron 86:665–71 [Google Scholar]
  102. Newton FG, zur Lage PI, Karak S, Moore DJ, Göpfert MC, Jarman AP. 102.  2012. Forkhead transcription factor Fd3F cooperates with Rfx to regulate a gene expression program for mechanosensory cilia specialization. Dev. Cell. 22:1221–33 [Google Scholar]
  103. Palghat Udayashankar A, Kössl M, Nowotny M. 103.  2012. Tonotopically arranged traveling waves in the miniature hearing organ of bushcrickets. PLOS ONE 7:e31008 [Google Scholar]
  104. Park J, Lee J, Shim J, Han W, Lee J. 104.  et al. 2013. dTULP, the Drosophila melanogaster homolog of tubby, regulates transient receptor potential channel localization in cilia. PLOS Genet. 9:e1003814 [Google Scholar]
  105. Pézier A, Jezzini SH, Marie B, Blagburn JM. 105.  2014. Engrailed alters the specificity of synaptic connections of Drosophila auditory neurons with the giant fiber. J. Neurosci. 34:11691–704 [Google Scholar]
  106. Pierce ML, Weston MD, Fritzsch B, Gabel HW, Ruvkun G, Soukup GA. 106.  2008. MicroRNA-183 family conservation and ciliated neurosensory organ expression. Evol. Dev. 10:106–13 [Google Scholar]
  107. Plotnick RE, Smith DM. 107.  2012. Exceptionally preserved fossil insect ears from the Eocene Green River Formation of Colorado. J. Palaeontol. 86:19–24 [Google Scholar]
  108. Pollack GS. 108.  1988. Selective attention in an insect auditory neuron. J. Neurosci. 8:2635–39 [Google Scholar]
  109. Pollack GS. 109.  1997. Neural processing of acoustic signals. Springer Handbook of Auditory Research 10 Comparative Hearing: Insects RR Hoy, AN Popper, RR Fay 138–96 New York: Springer [Google Scholar]
  110. Pollack GS. 110.  2015. Neurobiology of acoustically mediated predator detection. J. Comp. Physiol. A 201:99–109 [Google Scholar]
  111. Rabbitt RD, Brownell WE. 111.  2011. Efferent modulation of hair cell function. Curr. Opin. Otolaryngol. Head Neck Surg. 19:376–81 [Google Scholar]
  112. Reeve R, van Schaik A, Jin C, Hamilton T, Torben-Nielsen B, Webb B. 112.  2007. Directional hearing in a silicon cricket. Biosystems 87:307–13 [Google Scholar]
  113. Ren T. 113.  2002. Longitudinal pattern of basilar membrane vibration in the sensitive cochlea. PNAS 99:17101–6 [Google Scholar]
  114. Riabinina O, Dai M, Duke T, Albert JT. 114.  2011. Active process mediates species-specific tuning of Drosophila ears. Curr. Biol. 21:658–64 [Google Scholar]
  115. Robert D. 115.  2001. Innovative biomechanics for directional hearing in small flies. Biol. Bull. 200:190–94 [Google Scholar]
  116. Robert D, Göpfert MC. 116.  2002. Novel schemes for hearing and orientation in insects. Curr. Opin. Neurobiol. 12:715–20 [Google Scholar]
  117. Robles L, Ruggero MA. 117.  2001. Mechanics of the mammalian cochlea. Physiol. Rev. 81:1305–52 [Google Scholar]
  118. Roeder KD, Treat AE, Vandeberg JS. 118.  1968. Auditory sense in certain sphingid moths. Science 159:331–33 [Google Scholar]
  119. Roeder KD, Treat AE, Vande Berg JS. 119.  1970. Distal lobe of the pilifer: an ultrasonic receptor in choerocampine hawkmoths. Science 170:1098–99 [Google Scholar]
  120. Roemschied FA, Eberhard MJ, Schleimer JH, Ronacher B, Schreiber S. 120.  et al. 2014. Cell-intrinsic mechanisms of temperature compensation in a grasshopper sensory receptor neuron. eLife 8:e02078 [Google Scholar]
  121. Römer H. 121.  1983. Tonotopic organization of the auditory neuropile in the bushcricket Tettigonia viridissima. Nature 306:60–62 [Google Scholar]
  122. Römer H. 122.  2015. Directional hearing: from biophysical binaural cues to directional hearing outdoors. J. Comp. Physiol. A 201:87–97 [Google Scholar]
  123. Römer H, Bailey W. 123.  1996. Ecological constraints for the evolution of hearing and sound communication in insects. The Evolutionary Biology of Hearing DB Webster, RR Fay, AN Popper 79–93 New York: Springer [Google Scholar]
  124. Römer H, Krusch M. 124.  2000. A gain-control mechanism for processing of chorus sounds in the afferent auditory pathway of the bushcricket Tettigonia viridissima (Orthoptera, Tettigoniidae). J. Comp. Physiol. A 186:181–91 [Google Scholar]
  125. Ronacher B, Stumpner A. 125.  1988. Filtering of behaviourally relevant temporal parameters of a grasshopper's song by an auditory interneuron. J. Comp. Physiol. A 163:517–23 [Google Scholar]
  126. Roy M, Sivan-Loukianova E, Eberl DF. 126.  2013. Cell-type-specific roles of Na+/K+ ATPase subunits in Drosophila auditory mechanosensation. PNAS 110:181–86 [Google Scholar]
  127. Rust J, Stumpner A, Gottwald J. 127.  1999. Singing and hearing in a Tertiary bushcricket. Nature 399:650 [Google Scholar]
  128. Schnupp JWH, Nelken I, King AJ. 128.  2011. Auditory Neuroscience—Making Sense of Sound Cambridge, MA: MIT Press
  129. Schöneich S, Hedwig B. 129.  2010. Hyperacute directional hearing and phonotactic steering in the cricket (Gryllus bimaculatus deGeer). PLOS ONE 5:e15141 [Google Scholar]
  130. Schöneich S, Kostarakos K, Hedwig B. 130.  2015. An auditory feature detection circuit for sound pattern recognition. Sci. Adv. 1:e1500325 [Google Scholar]
  131. Senthilan PR, Piepenbrock D, Ovezmyradov G, Nadrowski B, Bechstedt S. 131.  et al. 2012. Drosophila auditory organ genes and genetic hearing defects. Cell 150:1042–54 [Google Scholar]
  132. Song L, McGee JA, Walsh EJ. 132.  2008. Development of cochlear amplification, frequency tuning, and two-tone suppression in the mouse. J. Neurophysiol. 99:344–55 [Google Scholar]
  133. Soulavie F, Piepenbrock D, Thomas J, Vieillard J, Duteyrat JL. 133.  et al. 2014. hemingway is required for sperm flagella assembly and ciliary motility in Drosophila. Mol. Biol. Cell 25:1276–86 [Google Scholar]
  134. Strauß J, Stumpner A. 134.  2015. Selective forces on origin, adaptation and reduction of tympanal ears in insects. J. Comp. Physiol. A 201:155–69 [Google Scholar]
  135. Stumpner A. 135.  1998. Picrotoxin eliminates frequency selectivity of an auditory interneuron in a bushcricket. J. Neurophysiol. 79:2408–15 [Google Scholar]
  136. Stumpner A, von Helversen D. 136.  2001. Evolution and function of auditory systems in insects. Naturwissenschaften 88:159–70 [Google Scholar]
  137. Sueur J, Windmill JF, Robert D. 137.  2006. Tuning the drum: the mechanical basis for frequency discrimination in a Mediterranean cicada. J. Exp. Biol. 209:4115–28 [Google Scholar]
  138. Surlykke A. 138.  1984. Hearing in notodontid moths: a tympanic organ with a single auditory neuron. J. Exp. Biol. 113:323–35 [Google Scholar]
  139. Teeling EC, Springer MS, Madsen O, Bates P, O'Brien SJ, Murphy WJ. 139.  2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–84 [Google Scholar]
  140. Tollin DJ. 140.  2003. The lateral superior olive: a functional role in sound source localization. Neuroscientist 9:127–43 [Google Scholar]
  141. Tollin DJ, Yin TCT. 141.  2002. The coding of spatial location by single units in the lateral superior olive of the cat. II. The determinants of spatial receptive fields in azimuth. J. Neurosci. 15:1468–79 [Google Scholar]
  142. van Staaden MJ, Römer H. 142.  1989. Evolutionary transition from stretch to hearing organs in ancient grasshoppers. Nature 394:773–76 [Google Scholar]
  143. Vigoder FDM, Ritchie MG, Gibson G, Peixoto AA. 143.  2013. Acoustic communication in insect disease vectors. Mem. Inst. Oswaldo Cruz 108:Suppl. 126–33 [Google Scholar]
  144. von Helversen D. 144.  1997. Acoustic communication and orientation in grasshoppers. Orientation and Communication in Arthropods M Lehrer 301–41 Basel, Switz.: Birkhäuser [Google Scholar]
  145. Warren B, Gibson G, Russell IJ. 145.  2009. Sex recognition through midflight mating duets in Culex mosquitoes is mediated by acoustic distortion. Curr. Biol. 19:485–91 [Google Scholar]
  146. Webb B, Wessnitzer J, Bush S, Schul J, Buchli J, Ijspeert A. 146.  2007. Resonant neurons and bushcricket behaviour. J. Comp. Physiol. A 193:285–88 [Google Scholar]
  147. Weber T, Göpfert MC, Winter H, Zimmermann U, Kohler H. 147.  et al. 2003. Expression of prestin-homologous solute carrier (SLC26) in auditory organs of nonmammalian vertebrates and insects. PNAS 100:7690–95 [Google Scholar]
  148. Windmill JF, Fullard JH, Robert D. 148.  2007. Mechanics of a ‘simple’ ear: tympanal vibrations in noctuid moths. J. Exp. Biol. 210:2637–48 [Google Scholar]
  149. Windmill JF, Göpfert MC, Robert D. 149.  2005. Tympanal travelling waves in migratory locusts. J. Exp. Biol. 208:157–68 [Google Scholar]
  150. Wyttenbach RA, May ML, Hoy RR. 150.  1996. Categorical perception of sound frequency by crickets. Science 273:1542–44 [Google Scholar]
  151. Xiong W, Grillet N, Elledge HM, Wagner TF, Zhao B. 151.  et al. 2012. TMHS is an integral component of the mechanotransduction machinery of cochlear hair cells. Cell 151:1283–95 [Google Scholar]
  152. Yack JE. 152.  2004. The structure and function of auditory chordotonal organs in insects. Microsc. Res. Tech. 63:315–37 [Google Scholar]
  153. Yager DD. 153.  1996. Serially homologous ears perform frequency range fractionation in the praying mantis, Creobroter (Mantodea, Hymenopodidae). J. Comp. Physiol. A 178:463–75 [Google Scholar]
  154. Yager DD. 154.  1999. Structure, development, and evolution of insect auditory systems. Microsc. Res. Tech. 47:380–400 [Google Scholar]
  155. Yager DD, Spangler HG. 155.  1997. Behavioral response to ultrasound by the tiger beetle Cicindela marutha Dow combines aerodynamic changes and sound production. J. Exp. Biol. 200:649–59 [Google Scholar]
  156. Yan Z, Zhang W, He Y, Gorczyca D, Xiang Y. 156.  et al. 2013. Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 493:221–25 [Google Scholar]
  157. Zanini D, Göpfert MC. 157.  2013. Mechanosensation: tethered ion channels. Curr. Biol. 23:R349–51 [Google Scholar]
  158. Zanini D, Göpfert MC. 158.  2014. TRPs in hearing. Handb. Exp. Pharmacol. 223:899–916 [Google Scholar]
  159. Zhang W, Cheng LE, Kittelmann M, Li J, Petkovic M. 159.  et al. 2015. Ankyrin repeats act as a tether for conveying force to gate the NOMPC mechanotransduction channel. Cell 162:1391–403 [Google Scholar]
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