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Selective forces on origin, adaptation and reduction of tympanal ears in insects

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Abstract

Insect ears evolved many times independently. As a consequence, a striking diversity exists in the location, construction and behavioural implementation of ears. In this review, we first summarise what is known about the evolutionary origin of ears and the presumed precursor organs in the various insect groups. Thereafter, we focus on selective forces for making and keeping an ear: we discuss detecting and localising predators and conspecifics, including establishing new “private” channels for intraspecific communication. More advanced aspects involve judging the distance of conspecifics, or assessing individual quality from songs which makes auditory processing a means for exerting sexual selection on mating partners. We try to identify negative selective forces, mainly in the context of energy expenditure for developing and keeping an ear, but also in conjunction with acoustic communication, which incorporates risks like eavesdropping by predators and parasitoids. We then discuss balancing pressures, which might oppose optimising an ear for a specific task (when it serves different functions, for example). Subsequently, we describe various scenarios that might have led to a reduction or complete loss of ears in evolution. Finally, we describe cases of sex differences in ears and potential reasons for their appearance.

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References

  • Atkins G, Pollack GS (1987) Response properties of prothoracic, interganglionic, sound-activated interneurons in the cricket Teleogryllus oceanicus. J Comp Physiol A 161:681–693

    Google Scholar 

  • Bailey WJ (1991) Acoustic behaviour of insects. An evolutionary perspective, Chapman and Hall London 225 p

    Google Scholar 

  • Bailey WJ (1998) Do large bushcrickets have more sensitive ears? Natural variation in hearing thresholds within populations of the bushcricket Requena verticalis (Listroscelidinae: Tettigoniidae). Physiol Entomol 23:105–112

    Google Scholar 

  • Bailey WJ, Haythornthwaite S (1998) Risks of calling by the field cricket Teleogryllus oceanicus; potential predation by Australian longeared bats. J Zool 244:505–513

    Google Scholar 

  • Bailey WJ, Kamien D (2001) Hearing dimorphism, trait variation and conflicts over space in the thorax of the bushcricket Requena verticalis (Listroscelidinae: Tettigoniidae: Orthoptera). J Comp Physiol A 187:647–652

    CAS  PubMed  Google Scholar 

  • Bailey WJ, Rentz DCF (eds) (1990) The Tettigoniidae: biology, systematics and evolution. Crawford House Press, Bathurst

    Google Scholar 

  • Bailey WJ, Römer H (1991) Sexual differences in auditory sensitivity: mismatch of hearing threshold and call frequency in a tettigoniid (Orthoptera, Tettigoniidae: Zaprochilinae). J Comp Physiol A 169:349–353

    Google Scholar 

  • Bailey WJ, Simmons LW (1991) Male-male interactions and sexual dimorphism in the ear of a zaprochiline tettigoniid. J Insect Behav 4:51–64

    Google Scholar 

  • Boyan GS (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 

  • Boyan G, Williams L, Fullard J (1990) Organization of the auditory pathway in the thoracic ganglia of noctuid moths. J Comp Neurol 295:248–267

    CAS  PubMed  Google Scholar 

  • Bruel & Kjaer (1995) Microphone handbook. Technical documentation for the Falcon TM range of microphone products. Downloaded from http://www.bruelkjaer.de. Accessed15 Oct 2014

  • Caldwell MS (2014) Interactions between airborne sound and substrate vibration in animal communication. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, Heidelberg, New York, pp 65–92

    Google Scholar 

  • Cardone B, Fullard JH (1988) Auditory characteristics and sexual dimorphism in the gypsy moth. Physiol Entomol 13:9–14

    Google Scholar 

  • Conner WE, Corcoran AJ (2012) Sound strategies: the 65-million-year-old battle between bats and insects. Annu Rev Entomol 57:21–39

    CAS  PubMed  Google Scholar 

  • Desutter-Grandcolas L (2003) Phylogeny and the evolution of acoustic communication in extant Ensifera (Insecta, Orthoptera). Zool Scripta 32:525–556

    Google Scholar 

  • Drosopoulos S, Claridge MF (eds) (2006) Insect Sounds and communication: physiology, behaviour, ecology, and evolution. CRC Press, Boca Raton

  • Farris HE, Oshinsky ML, Forrest TG, Hoy RR (2008) Auditory sensitivity of an acoustic parasitoid (Emblemasoma sp., Sarcophagidae, Diptera) and the calling behavior of potential hosts. Brain Behav Evol 72:16–26

    CAS  PubMed Central  PubMed  Google Scholar 

  • Field LH, Matheson T (1998) Chordotonal organs of insects. Adv Insect Physiol 27:1–228

    Google Scholar 

  • Flook PK, Rowell CHF (1998) Inferences about orthopteroid phylogeny and molecular evolution from small subunit nuclear ribosomal DNA sequences. Insect Mol Biol 7:163–178

    CAS  PubMed  Google Scholar 

  • Flook PK, Klee S, Rowell CHF (2000) Molecular phylogenetic analysis of the Pneumoroidea (Orthoptera, Caelifera): molecular data resolve morphological character conflicts in the basal Acridomorpha. Mol Phyl Evol 15:345–354

    CAS  Google Scholar 

  • Fong DW, Kane TC, Culver DC (1995) Vestigialization and loss of nonfunctional characters. Ann Rev Ecol Syst 26:249–268

    Google Scholar 

  • Fonseca P (2014) Cicada acoustic communication. In: Hedwig B (ed) Insect hearing and acoustic communication. Springer, New York, pp 101–121

    Google Scholar 

  • Fournier JP, Dawson JW, Mikhail A, Yack JE (2013) If a bird flies in the forest, does an insect hear it? Biol Lett 9:20130319

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fullard JH (1990) The sensory ecology of moths and bats: global lessons in staying alive. In: Evans DL, Schmidt JO (eds) Insect defences. Adaptive mechanisms and strategies of prey and predators. State University of New York Press, Albany, pp 203–226

    Google Scholar 

  • Fullard JH (1994) Auditory changes in noctuid moths endemic to a bat-free habitat. J Evol Biol 7:435–445

    Google Scholar 

  • Fullard JH (1998) The sensory coevolution of moths and bats. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, New York, pp 279–326

    Google Scholar 

  • Fullard JH, Dawson JW (1999) Why do diurnal moths have ears? Naturwissenschaften 86:276–279

    CAS  Google Scholar 

  • Fullard JH, Yack JE (1993) The evolutionary biology of insect hearing. Trends Ecol Evol 8:248–252

    CAS  PubMed  Google Scholar 

  • Fullard JH, Dawson JW, Otero LD, Surlykke A (1997) Bat-deafness in day-flying moths (Lepidoptera, Notodontidae, Dioptinae). J Comp Physiol A 181:477–483

    CAS  PubMed  Google Scholar 

  • Fullard JH, Ratcliffe JM, Soutar AR (2004) Extinction of the acoustic startle response in moths endemic to a bat-free habitat. J Evol Biol 17:856–861

    CAS  PubMed  Google Scholar 

  • Fullard JH, Ratcliffe JM, ter Hofstede H (2007) Neural evolution in the bat-free habitat of Tahiti: partial regression in an anti-predator auditory system. Biol Lett 22:26–2

  • Fullard JH, ter Hofstede HM, Ratcliffe JM, Pollack GS, Brigidi GS, Tinghitella RM, Zuk M (2010) Release from bats: genetic distance and sensoribehavioural regression in the Pacific field cricket, Teleogryllus oceanicus. Naturwissenschaften 97:53–61

    CAS  PubMed  Google Scholar 

  • Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: Common problems and diverse solutions. Chicago University Press, Chicago

    Google Scholar 

  • Gill PG, Purnell MA, Crumpton N, Brown KR, Gostling NJ, Stampanoni M, Rayfield EJ (2014) Dietary specializations and diversity in feeding ecology of the earliest stem mammals. Nature 512:303–305

    CAS  PubMed  Google Scholar 

  • Greenfield MD (2002) Signalers and receivers. Mechanisms and evolution of arthropod communication. Oxford University Press, Oxford 432 p

    Google Scholar 

  • Greenfield MD (2014) Acoustic communication in the nocturnal Lepidoptera. In: Hedwig B (ed) Insect hearing and acoustic communication. Springer, New York, pp 81–100

    Google Scholar 

  • Greenfield M, Hohendorf H (2009) Independence of sexual and anti-predator perceptual functions in an acoustic moth: implications for the receiver bias mechanism in signal evolution. Ethology 115:1137–1149

    Google Scholar 

  • Gu J-J, Montealegre-Z F, Robert D, Engel MS, Qiao G-X, Ren D (2012) Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females. Proc Natl Acad Sci USA 109:3868–3873

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gwynne DT, Bailey WJ (1999) Female-female competition in katydids: sexual selection for increased sensitivity to a male signal? Evolution 53:546–551

    Google Scholar 

  • Hardt M, Watson AHD (1994) Distribution of synapses on two ascending interneurones carrying frequency-specific information in the auditory system of the cricket: evidence for GABAergic input. J Comp Neurol 345:481–495

    CAS  PubMed  Google Scholar 

  • Harrison SJ, Thomson IR, Grant CM, Bertram SM (2013) Calling, courtship, and condition in the fall field cricket, Gryllus pennsylvanicus. PLoS ONE 8(3):e60356. doi:10.1371/journal.pone.0060356

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hasenfuss I (1997) Precursor structures and evolution of tympanal organs in Lepidoptera (Insecta, Pterygota). Zoomorphology 117:155–164

    Google Scholar 

  • Hasenfuss I (2000) Evolutionary pathways of truncal tympanal organs in Lepidoptera (Insecta: Holometabola). Zool Anz 239:27–44

    Google Scholar 

  • Hedwig B (ed) (2014) Insect hearing and acoustic communication. Springer, New York

    Google Scholar 

  • Heitmann H (1934) Die Tympanalorgane flugunfähiger Lepidopteren und die Korrelation in der Ausbildung der Flügel und der Tympanalorgane. Zool Jb Abt Anat Ontog 59:135–200

    Google Scholar 

  • Heller K-G (1984) To the bioacoustics and phylogeny of the genus Poecilimon (Orthoptera, Tettigoniidae, Phaneropterinae). Zool Jb Syst 111:69–117

    Google Scholar 

  • Heller K-G (1990) Evolution of song pattern in east Mediterranean Phaneropterinae: constraints by the communication system. In: Bailey WJ, Rentz DCF (eds) The Tettigoniidae: Biology, systematics and evolution. Crawford House Press, Bathurst, pp 130–151

    Google Scholar 

  • Heller K-G, Schul J, Ingrisch S (1997) Sex-specific differences in song frequency and tuning of the ears in some duetting bushcrickets (Orthoptera: Tettigonioidea: Phaneropteridae). Zoology 100:110–118

    Google Scholar 

  • Höbel G, Schul J (2007) Listening for males and bats: spectral processing in the hearing organ of Neoconocephalus bivocatus (Orthoptera: Tettigoniidae). J Comp Physiol A 193:917–925

    Google Scholar 

  • Hoffmann E, Jatho M (1995) The acoustic trachea of Tettigoniids as an exponential horn: theoretical calculations and bioacoustical measurements. J Acoust Soc Am 98:1845–1851

    Google Scholar 

  • Hoy RR (1992) The evolution of hearing in insects as an adaptation to predation from bats. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 115–129

    Google Scholar 

  • Hoy RR, Robert D (1996) Tympanal hearing in insects. Annu Rev Entomol 41:433–450

    CAS  PubMed  Google Scholar 

  • Hoy RR, Popper AN, Fay RR (eds) (1998) Comparative hearing: insects. Springer, New York

    Google Scholar 

  • Huber F, Moore TE, Loher E (eds) (1989) Cricket behaviour and neurobiology. Cornell University Press, Ithaca

  • Jacobs DS, Ratcliffe JM, Fullard JH (2008) Beware of bats, beware of birds: the auditory responses of eared moths to bat and bird predation. Behav Ecol 19(6):1333–1342

    Google Scholar 

  • Jain M, Diwakar S, Bahuleyan J, Deb R, Balakrishnan R (2014) A rain forest dusk chorus: cacophony or sounds of silence? Evol Ecol 28:1–22

    Google Scholar 

  • Jeffery WR (2005) Adaptive evolution of eye degeneration in the Mexican blind cavefish. J Hered 96:185–196

    CAS  PubMed  Google Scholar 

  • Jeram S, Rössler W, Čokl A, Kalmring K (1995) Structure of atympanate tibial organs in legs of the cave-living Ensifera, Troglophilus neglectus (Gryllacridoidea, Raphidophoridae). J Morphol 223:109–118

    Google Scholar 

  • Jones PL, Ryan MJ, Page RA (2014) Population and seasonal variation in response to prey calls by an eavesdropping bat. Behav Ecol Sociobiol 68:605–615

    Google Scholar 

  • Kalmring K, Sickmann T, Jatho M, Zhantiev R, Grossbach M (1997) The auditory- vibratory sensory system of the bushcricket Polysarcus denticauda. (Phaneropterinae, Tettigoniidae) III. Physiology of the ventral chord neurons ascending to the head ganglia. J Exp Zool 279:9–28

    Google Scholar 

  • Keil TA (1997) Functional morphology of insect mechanoreceptors. Microsc Res Tech 39:506–531

    CAS  PubMed  Google Scholar 

  • Klaus S, Mendoza JC, Liew JH, Plath M, Meier R, Yeo DC (2013) Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs. Biol Lett 9:20121098

    PubMed Central  PubMed  Google Scholar 

  • Kostarakos K, Hartbauer M, Römer H (2008) Matched filters, mate choice and the evolution of sexually selected traits. PLoS ONE 3(8):e3005

    PubMed Central  PubMed  Google Scholar 

  • Kostarakos K, Hennig M, Römer H (2009) Two matched filters and the evolution of mating signals in four species of cricket. Front Zool 6:22

    PubMed Central  PubMed  Google Scholar 

  • Kristensen NP (2012) Molecular phylogenies, morphological homologies and the evolution of moth ‘ears’. Syst Entomol 37:237–239

    Google Scholar 

  • Kühne R (1982) Neurophysiology of the vibratory sense in locusts and bushrickets: the responses of ventral-cord neurones. J Insect Physiol 28:615–623

    Google Scholar 

  • Lakes R, Schikorski T (1990) Neuroanatomy of the tettigoniids. In: Bailey WJ, Rentz DCF (eds) The Tettigoniidae: Biology, systematics and evolution. Crawford House Press, Bathurst, pp 166–190

    Google Scholar 

  • Lakes-Harlan R, Bailey WW, Schikorski T (1991) The auditory system of an atympanate bushcricket Phasmodes ranatriformes (Westwood) (Tettigoniidae: Orthoptera). J Exp Biol 158:307–324

    Google Scholar 

  • Lakes-Harlan R, Stölting H, Stumpner A (1999) Convergent evolution of insect hearing organs from a preadaptive structure. Proc R Soc London B 266:1161–1167

    Google Scholar 

  • Lakes-Harlan R, Jacobs K, Allen G (2007) Comparison of auditory sense organs in parasitoid Tachinidae (Diptera) hosted by Tettigoniidae (Orthoptera) and homologous structures in an non-hearing Phoridae (Diptera). Zoomorphology 126:229–243

    Google Scholar 

  • Lakes-Harlan R, deVries T, Stölting H, Stumpner A (2014) Useless hearing in male Emblemasoma auditrix (Diptera, Sarcophagidae)–a case of intralocus sexual conflict during evolution of a complex sense organ? PLoS ONE 9(1):e87211

    PubMed Central  PubMed  Google Scholar 

  • Lane KA, Lucas KM, Yack JE (2008) Hearing in a diurnal, mute butterfly, Morpho peleides (Papilionoidea, Nymphalidae). J Comp Neurol 508:677–686

    PubMed  Google Scholar 

  • Latimer W, Schatral A (1983) The acoustic behaviour of the bush cricket Tettigonia cantans. I. Behavioural responses to sound and vibration. Behav Proc 8:113–124

    CAS  Google Scholar 

  • Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475–480

    CAS  PubMed  Google Scholar 

  • Lee MS, Cau A, Naish D, Dyke GJ (2014) Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345:562–566

    CAS  PubMed  Google Scholar 

  • Lehmann GUC, Strauß J, Lakes-Harlan R (2007) Listening when there is no sexual signalling? Maintenance of hearing in the asexual bushcricket Poecilimon intermedius. J Comp Physiol A 193:537–545

    Google Scholar 

  • Lehmann GUC, Berger S, Strauß J, Lehmann AW, Pflüger JH (2010) The auditory system of non-calling grasshoppers (Melanoplinae: Podismini) and the evolutionary regression of their tympanal ears. J Comp Physiol A 196:807–816

    Google Scholar 

  • Lewis DB (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 60:821–837

    CAS  PubMed  Google Scholar 

  • Machens CK, Schütze H, Franz A, Kolesnikova O, Stemmler MB, Ronacher B, Herz AV (2003) Single auditory neurons rapidly discriminate conspecific communication signals. Nat Neurosci 6:341–342

    CAS  PubMed  Google Scholar 

  • Mason AC (1991) Hearing in a primitive ensiferan: the auditory system of Cyphoderris monstrosa (Orthoptera: Haglidae). J Comp Physiol A 168:351–363

    Google Scholar 

  • Mason AC, Faure PA (2004) The physiology of insect auditory afferents. Microsc Res Tech 63:338–350

    PubMed  Google Scholar 

  • Mason AC, Morris GK, Hoy RR (1999) Peripheral frequency mis-match in the primitive ensiferan Cyphoderris monstrosa (Orthoptera: Haglidae). J Comp Physiol A 184:432–551

    Google Scholar 

  • Mason AC, Oshinsky ML, Hoy RR (2001) Hyperacute directional hearing in a microscale auditory system. Nature 410:686–690

    CAS  PubMed  Google Scholar 

  • Meier T, Reichert H (1990) Embryonic development and evolutionary origin of the orthopteran auditory organs. J Neurobiol 21:592–610

    CAS  PubMed  Google Scholar 

  • Meyer J, Elsner E (1996) How well are frequency sensitivities of grasshopper ears tuned to species-specific song spectra? J Exp Biol 199:1631–1642

    PubMed  Google Scholar 

  • Michelsen A, Heller KG, Stumpner A, Rohrseitz K (1994) A new biophysical method to determine the gain of the acoustic trachea in bushcrickets. J Comp Physiol A 175:145–151

    CAS  PubMed  Google Scholar 

  • Miller LA (1970) Structure of the green lacewing tympanal organ (Chrysopa carnea, Neuroptera). J Morphol 131:359–382

    Google Scholar 

  • Miller LA, Olesen J (1979) Avoidance behavior in green lacewings: I. Behavior of free flying green lacewings to hunting bats and ultrasound. J Comp Physiol A 131:113–120

    Google Scholar 

  • Miller LA, Surlykke A (2001) How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator. Bioscience 51:570–581

    Google Scholar 

  • Moir HM, Jackson JC, Windmill JF (2013) Extremely high frequency sensitivity in a ‘simple’ ear. Biol Lett 9(4):20130241

    PubMed Central  PubMed  Google Scholar 

  • Mowles SL (2014) The physiological cost of courtship: field cricket song results in anaerobic metabolism. Anim Behav 89:39–43

    Google Scholar 

  • Muma KE, Fullard JH (2004) Persistence and regression of hearing in the exclusively diurnal moths, Trichodezia albovittata (Geometridae) and Lycomorpha pholus (Arctiidae). Ecol Entomol 29:718–726

    Google Scholar 

  • Nakano R, Takanashi T, Skals N, Surlykke A, Ishikawa Y (2010) To females of a noctuid moth, male courtship songs are nothing more than bat echolocation calls. Biol Lett 6:582–584

    PubMed Central  PubMed  Google Scholar 

  • Nakano R, Takanashi T, Surlykke A, Skals N, Ishikawa Y (2013) Evolution of deceptive and true courtship songs in moths. Sci Rep 3:2003

    PubMed Central  PubMed  Google Scholar 

  • Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804

    CAS  PubMed  Google Scholar 

  • Otte D (1990) The relation between hearing and flying in insects. Ent News 101:29–34

    Google Scholar 

  • Otte D, Peck SB (1998) A new blind Anurogryllus from the Galapagos Islands, Ecuador (Orthoptera: Gryllidae: Brachytrupinae). J Orthoptera Res 7:227–230

    Google Scholar 

  • Pearson KG, Hedwig B, Wolf H (1989) Are the hind wing chordotonal organs of the locust elements in the flight pattern generator? J Exp Biol 144:235–255

    Google Scholar 

  • Pflüger H-J, Field LH (1999) A thoracic chordotonal organ in locusts which codes for mechanical and acoustic stimuli. J Comp Physiol A 184:169–183

    Google Scholar 

  • Pires A, Hoy RR (1992) Temperature coupling in cricket acoustic communication. I. Field and laboratory studies of temperature effects on calling song production and recognition in Gryllus firmus. J Comp Physiol A 171:69–78

    CAS  PubMed  Google Scholar 

  • Pollack GS, Imaizumi K (1999) Neural analysis of sound frequency in insects. BioEssays 21:295–303

    Google Scholar 

  • Pollack GS, Martins R (2007) Flight and hearing: ultrasound sensitivity differs between flight-capable and flight-incapable morphs of a wing-dimorphic cricket species. J Exp Biol 210:3160–3164

    PubMed  Google Scholar 

  • Prager (1973) Die Hörschwelle des mesothorakalen Tympanalorgans von Corixa punctata III. (Heteroptera, Corixidae). J Comp Physiol 86:55–58

    Google Scholar 

  • Prestwich KN, O’Sullivan K (2005) Simultaneous measurement of metabolic and acoustic power and the efficiency of sound production in two mole cricket species (Orthoptera: Gryllotalpidae). J Exp Biol 208:1495–1512

    PubMed  Google Scholar 

  • Prier KR, Boyan GS (2000) Synaptic input from serial chordotonal organs onto segmentally homologous interneurons in the grasshopper Schistocerca gregaria. J Insect Physiol 46:297–312

    CAS  PubMed  Google Scholar 

  • Rajamaran K, Mhatre N, Jain M, Postles M, Balakrishnan R, Robert D (2013) Low-pass filters and differential tympanal tuning in a palaeotropical bushcricket with an unusually low frequency call. J Exp Biol 216:777–787

    Google Scholar 

  • Rantala MJ, Kortet R (2003) Courtship song and immune function in the field cricket Gryllus bimaculatus. Biol J Linn Soc 79:503–510

    Google Scholar 

  • Rétaux S, Casane D (2013) Evolution of eye development in the darkness of caves: adaptation, drift, or both? EvoDevo 4:26

    PubMed Central  PubMed  Google Scholar 

  • Rheinlaender J, Römer H (1990) Acoustic cues for sound localisation and spacing in Orthopteran insects. In: BaileyWJ, Rentz DCF (eds) The Tettigoniidae: biology, systematics and evolution. Crawford House Press, Bathurst, pp 248–264

  • Riede K, Kämper G, Höfler I (1990) Tympana, auditory thresholds, and projection areas of tympanal nerves in singing and silent grasshoppers (Insecta, Acrididae). Zoomorphology 109:223–230

    Google Scholar 

  • Ritzmann RE, Pollack AJ, Hudson SE, Hyvonen A (1991) Convergence of multi-modal sensory signals at thoracic interneurons of the escape system of the cockroach, Periplaneta americana. Brain Res 563:175–183

    CAS  PubMed  Google Scholar 

  • Robert D, Edgecomb RS, Read MP, Hoy RR (1996) Tympanal hearing in tachinid flies (Diptera, Tachinidae, Ormiini): the comparative morphology of an innovation. Cell Tissue Res 284:435–448

    CAS  PubMed  Google Scholar 

  • Robinson DJ, Hall MJ (2002) Sound signalling in Orthoptera. Adv Insect Physiol 29:151–278

    Google Scholar 

  • Rodriguez RL, Greenfield MD (2004) Behavioural context regulates dual function of ultrasonic hearing in lesser waxmoth: bat avoidance and pair formation. Physiol Entomol 29:159–168

    Google Scholar 

  • Römer H (1993) Environmental and biological constraints for the evolution of long-range signalling and hearing in acoustic insects. Trans R Soc Lond B 226:179–185

    Google Scholar 

  • Römer H, Smith AR, van Staaden M (2014) Hearing and sensory ecology of acoustic communication in bladder grasshoppers. In: Hedwig B (ed) Insect hearing and acoustic communication. Springer, New York, pp 27–43

    Google Scholar 

  • Rössler W (1992) Functional morphology and development of tibial organs in the legs I, II and III of the bushcricket Ephippiger ephippiger (Insecta, Ensifera). Zoomorphology 112:181–188

  • Rowland EP, Schaefer W, Belton P, Gries G (2011) Evidence for short-range sonic communication in lyman-triine moths. J Insect Physiol 57:292–299

    CAS  PubMed  Google Scholar 

  • Schmidt AK, Römer H (2011) Solutions to the cocktail party problem in insects: selective filters, spatial release from masking and gain control in tropical crickets. PLoS ONE 6(12):e28593

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schmidt AK, Riede K, Römer H (2011) High background noise shapes selective auditory filters in a tropical cricket. J Exp Biol 214:1754–1762

    PubMed Central  PubMed  Google Scholar 

  • Schmidt AKD, Römer H, Riede K (2013) Spectral niche segregation and community organization in a tropical cricket assemblage. Behav Ecol 24:470–480

    Google Scholar 

  • Schnupp JW, Carr CE (2009) On hearing with more than one ear: lessons from evolution. Nat Neurosci 12:692–697

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schöneich S, Hedwig B (2010) Hyperacute directional hearing and phonotactic steering in the cricket (Gryllus bimaculatus deGeer). PLoS ONE 5:e15141

    PubMed Central  PubMed  Google Scholar 

  • Schul J, Patterson AC (2003) What determines the tuning of hearing organs and the frequency of calls? A comparative study in the katydid genus Neoconocephalus (Orthoptera, Tettigoniidae). J Exp Biol 206:141–152

    PubMed  Google Scholar 

  • Shaw S (1994) Detection of airborne sound by a cockroach ‘vibration’ detector: a possible missing link in insect auditory evolution. J Exp Biol 193:13–47

    PubMed  Google Scholar 

  • Simmons LW, Thomas ML, Simmons FW, Zuk M (2013) Female preferences for acoustic and olfactory signals during courtship: male crickets send multiple messages. Behav Ecol 24:1099–1107

    Google Scholar 

  • Skals N, Anderson P, Kanneworff M, Löfstedt C, Surlykke A (2005) Her odours make him deaf: crossmodal modulation of olfaction and hearing in a male moth. J Exp Biol 208:595–601

    PubMed  Google Scholar 

  • Stölting H, Moore TE, Lakes-Harlan R (2002) Substrate vibrations during acoustic signalling in the cicada Okagana rimosa. J Insect Sci 2:2

    PubMed Central  PubMed  Google Scholar 

  • Stölting H, Moore TE, Lakes-Harlan R (2004) Acoustic communication in Okanagana rimosa (Say) (Homoptera: Cicadidae). Zoology 107:243–257

    PubMed  Google Scholar 

  • Stölting H, Stumpner A, Lakes-Harlan R (2007) Morphology and physiology of the prosternal chordotonal organ of the sarcophagid fly Sarcophaga bullata (Parker). J Insect Physiol 53:444–454

    PubMed  Google Scholar 

  • Strauß J, Lakes-Harlan R (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 71:167–180

    PubMed  Google Scholar 

  • Strauß J, Lakes-Harlan R (2009) The evolutionary origin of auditory receptors in Tettigonioidea: the complex tibial organ of Schizodactylidae. Naturwissenschaften 96:143–146

    PubMed  Google Scholar 

  • Strauß J, Lakes-Harlan R (2014) Evolutionary and phylogenetic origins of tympanal hearing organs in insects. In: Hedwig B (ed) Insect hearing and acoustic communication. Springer, New York, pp 5–26

    Google Scholar 

  • Strauß J, Lehmann AW, Lehmann GUC (2014a) Sensory evolution of hearing in tettigoniids with differing communication systems. J Evol Biol 27:200–213

    Google Scholar 

  • Strauß J, Stritih N, Lakes-Harlan R (2014b) The subgenual organ complex in the cave cricket Troglophilus neglectus (Orthoptera: Rhaphidophoridae): comparative innervation and sensory evolution. R Soc Open Sci 1:140240

    Google Scholar 

  • Stritih N, Čokl A (2014) The role of frequency in vibrational communication of Orthoptera. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, New York, pp 375–393

    Google Scholar 

  • Stritih N, Stumpner A (2009) Vibratory interneurons in the non-hearing cave cricket indicate evolutionary origin of sound processing elements in Ensifera. Zoology 112:48–68

    PubMed  Google Scholar 

  • Strümpel H (2005) Ordnung Auchenorrhyncha, Zikaden. In: Dathe HH (ed) Lehrbuch der Speziellen Zoologie, Band I: Wirbellose. 5. Teil: Insecta. Spektrum, Heidelberg, Berlin, pp 346–365

  • Stumpner A (1999) An interneurone of unusual morphology is tuned to the female song in the bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J Exp Biol 202:2071–2081

    CAS  PubMed  Google Scholar 

  • Stumpner A (2002) A species-specific frequency filter through specific inhibition, not specific excitation. J Comp Physiol A 188:239–248

    CAS  Google Scholar 

  • Stumpner A, Heller K (1992) Morphological and physiological differences of the auditory system in three related bushcrickets (Orthoptera: Phaneropteridae, Poecilimon). Physiol Entomol 17:73–80

    Google Scholar 

  • Stumpner A, Nowotny M (2014) Neural processing in the bush-cricket auditory pathway. In: Hedwig B (ed) Insect hearing and acoustic communication. Springer, New York, pp 143–166

    Google Scholar 

  • Stumpner A, von Helversen D (2001) Evolution and function of auditory system in insects. Naturwissenschaften 88:159–170

    CAS  PubMed  Google Scholar 

  • Sueur J (2002) Cicada acoustic communication: potential sound partitioning in a multispecies community from Mexico (Hemiptera: Cicadomorpha: Cicadidae). Biol J Linn Soc 75:379–394

    Google Scholar 

  • Sueur J, Windmill JF, Robert D (2008) Sexual dimorphism in auditory mechanics: tympanal vibrations of Cicada orni. J Exp Biol 211:2379–2387

    PubMed  Google Scholar 

  • Surlykke A, Skals N, Rydell J, Svensson M (1998) Sonic hearing in a diurnal geometrid moth, Archiearis parthenias, temporally isolated from bats. Naturwissenschaften 85:36–37

    CAS  Google Scholar 

  • Takanashi T, Nakano R, Surlykke A, Tatsuta H, Tabata J, Ishikawa Y, Skals N (2010) Variation in courtship ultrasounds of three Ostrinia moths with different sex pheromones. PLoS ONE 5(10):e13144

    PubMed Central  PubMed  Google Scholar 

  • Teeling EC, Dool S, Springer MS (2012) Phylogenies, fossils and functional genes: the evolution of echolocation in bats. In: Gunnell GF, Simmons NB (eds) Evolutionary history of bats. Fossils, molecules and morphology. Cambridge University Press, Cambridge, pp 1–22

  • ter Hofstede HM, Ratcliff JM, Fullard JH (2008) Nocturnal activity positively correlated with auditory sensitivity in noctuoid moths. Biol Lett 4:262–265

    PubMed Central  PubMed  Google Scholar 

  • ter Hofstede HM, Goerlitz HR, Ratcliffe JM, Holderied MW, Surlykke A (2013) The simple ears of noctuoid moths are tuned to the calls of their sympatric bat community. J Exp Biol 216:3954–3962

    PubMed  Google Scholar 

  • Triblehorn JD, Yager DD (2005) Timing of praying mantis evasive responses during simulated bat attack sequences. J Exp Biol 208:1867–1876

    PubMed  Google Scholar 

  • Triblehorn JD, Ghose K, Bohn K, Moss CF, Yager DD (2008) Free-flight encounters between praying mantids (Parasphendale agrionina) and bats (Eptesicus fuscus). J Exp Biol 211:555–562

    CAS  PubMed  Google Scholar 

  • van Staaden MJ, Römer H (1998) Evolutionary transition from stretch to hearing in ancient grasshoppers. Nature 394:773–776

    Google Scholar 

  • von Helversen D, von Helversen O, Heller K-G (2012) When to give up responding acoustically in Poecilimon bushcrickets: a clue to population density. Articulata 27:57–66

    Google Scholar 

  • Wessel A, Mühlethaler R, Hartung V, Kuštor V, Gogala M (2014) The tymbal: Evolution of a complex vibration-producing organ in the Tymbalia (Hemiptera excl. Stenorrhyncha). In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, Heidelberg, New York, pp 395–444

    Google Scholar 

  • Wiley C, Ellison CK, Shaw KL (2012) Widespread genetic linkage of mating signals and preferences in the Hawaiian cricket Laupala. Proc R Soc B 279:1203–1209

    PubMed Central  PubMed  Google Scholar 

  • Wyttenbach RA, May ML, Hoy RR (1996) Categorical perception of sound frequency by crickets. Science 273:1542–1544

    CAS  PubMed  Google Scholar 

  • Yack JE (2004) The structure and function of auditory chordotonal organs in insects. Microsc Res Tech 63:315–337

    PubMed  Google Scholar 

  • Yack JE, Fullard JH (1990) The mechanoreceptive origin of insect tympanal organs: a comparative study of similar nerves in tympanate and atympanate moths. J Comp Neurol 300:523–553

    CAS  PubMed  Google Scholar 

  • Yack JE, Fullard JH (1993) What is an insect ear? Ann Entomol Soc America 86:677–682

    Google Scholar 

  • Yack JE, Fullard JH (2000) Ultrasonic hearing in nocturnal butterflies. Nature 403:265–266

    CAS  PubMed  Google Scholar 

  • Yack JE, Roots BI (1992) The metathoracic wing-hinge chordotonal organ of an atympanate moth, Actias luna (Lepidoptera, Saturniidae): a light- and electron-microscopic study. Cell Tissue Res 267:455–471

    CAS  PubMed  Google Scholar 

  • Yack JE, Scudder GGE, Fullard JH (1999) Evolution of the metathoracic tympanal ear and its mesothoracic homologue in the Macrolepidoptera (Insecta). Zoomorphology 119:93–103

    Google Scholar 

  • Yager DD (1990) Sexual dimorphism of auditory function and structure in praying mantises Mantodea; Dictyoptera. J Zool 221:517–537

    Google Scholar 

  • Yager DD (1999) Structure, development, and evolution of insect auditory systems. Microsc Res Tech 47:380–400

    CAS  PubMed  Google Scholar 

  • Yager DD (2005) Cockroach homologs of praying mantis peripheral auditory system components. J Morphol 265:120–139

    PubMed  Google Scholar 

  • Yager DD (2012) Predator detection and evasion by flying insects. Curr Opin Neurobiol 22:201–207

    CAS  PubMed  Google Scholar 

  • Yager DD, Svenson GJ (2008) Patterns of praying mantis auditory system evolution based on morphological, molecular, neurophysiological, and behavioural data. Biol J Linn Soc 94:541–568

    Google Scholar 

  • Young J, Walker SM, Bomphrey RJ, Taylor GK, Thomas ALR (2009) Details of insect wing design and deformation enhance aerodynamic function and flight efficiency. Science 325:1549–1552  

  • Zimmermann U, Rheinlaender J, Robinson D (1989) Cues for male phonotaxis in the duetting bushcricket Leptophyes punctatissima. J Comp Physiol A 164:621–628

    Google Scholar 

  • Zuk M, Rotenberry JT, Tinghitella RM (2006) Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biol Lett 2:521–524

    PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We want to thank Nataša Stritih, NIB Ljubljana, Slovenia, for discussions of the topic and comments on the manuscript. Bernd Ronacher and two anonymous reviewers helped with many thoughtful comments. We thank Ben Warren for numerous suggestions for improving the English that we hopefully were able to observe adequately.

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  1. Institute for Animal Physiology, AG Integrative Sensory Physiology, Justus-Liebig-Universität Gießen, Gießen, Germany

    Johannes Strauß

  2. Department of Cellular Neurobiology, JFB-Institute for Zoology and Anthropology, Georg-August-University of Göttingen, Schwann-Schleiden-Forschungszentrum, Julia-Lermontowa-Weg 3, 37077, Göttingen, Germany

    Andreas Stumpner

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Strauß, J., Stumpner, A. Selective forces on origin, adaptation and reduction of tympanal ears in insects. J Comp Physiol A 201, 155–169 (2015). https://doi.org/10.1007/s00359-014-0962-7

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