Skip to main content
SpringerLink
Log in

Evolutionary and Phylogenetic Origins of Tympanal Hearing Organs in Insects

  • Chapter
  • First Online:
Insect Hearing and Acoustic Communication

Part of the book series: Animal Signals and Communication ((ANISIGCOM,volume 1))

Abstract

Among insects, tympanal ears evolved at least 18 times, resulting in a diversity of auditory systems. Insects use their ears in different behavioural contexts, mainly intraspecific communication for mate attraction, predator avoidance, and parasitic host localisation. Analysing the evolution of insect ears aims at revealing the phyletic origins of auditory organs, the selection pressures leading to the evolution of ears, the physiological and behavioural adaptations of hearing, and the diversification of ears in specific groups or lineages. The origin of sensory organs from preadapted proprioceptive or vibroceptive organs has now been established for different ear types. In this review, we embed research on insect hearing in a phylogenetic framework to reconstruct the ancestral sensory situation in different taxa, and the series of morphological changes during the evolution of an ear. The importance of sensory and neuroanatomical data is discussed for either mapping onto a phylogeny or as characters for phylogenetic analysis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Arntz B (1975) Das Hörvermögen von Nepa cinerea L. Zur Funktionsweise der thorakalen Scolopalorgane. J Comp Physiol 96:53–72

    Article  Google Scholar 

  • Bailey WJ (1993) The tettigoniid (Orthoptera: Tettigoniidae) ear: multiple functions and structural diversity. Int J Insect Morphol Embryol 22:185–205

    Article  Google Scholar 

  • Boyan GS (1993) Another look at insect audition: the tympanic receptors as an evolutionary specialisation of the chordotonal system. J Insect Physiol 39:187–200

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Christensen-Dalsgaard J, Carr CE (2008) Evolution of a sensory novelty: tympanic ears and the associated neural processing. Brain Res Bull 75:365–370

    Article  PubMed  Google Scholar 

  • Claridge MF, Morgan JC, Moulds MS (1999) Substrate-transmitted acoustic signals of the primitive cicada, Tettigarcta crinita Distant (Hemiptera Cicadoidea, Tettigarctidae). J Nat Hist 33:1831–1834

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Desutter-Grandcolas L (2003) Phylogeny and the evolution of acoustic communication in extant Ensifera (Insecta, Orthoptera). Zool Scripta 32:525–561

    Article  Google Scholar 

  • Desutter-Grandcolas L, Legendre F, Grandcolas P, Robillard T, Murienne J (2005) Convergence and parallelism: is a new life ahead of old concepts? Cladistics 21:51–61

    Article  Google Scholar 

  • Doolan JM, Young D (1981) The organization of the auditory organ of the bladder cicada, Cystosoma saundersii. Phil Trans R Soc Lond B 291:525–540

    Article  Google Scholar 

  • Edgecomb RS, Robert D, Read MP, Hoy RR (1995) The tympanal organ of a fly: phylogenetic analysis of its morphological origin. Cell Tissue Res 282:251–268

    Article  PubMed  CAS  Google Scholar 

  • Field LH, Bailey WJ (1997) Sound production in primitive Orthoptera from Western Australia: sounds used in defence and social communication in Ametrus sp. and Hadrogryllacris sp. (Gryllacrididae: Orthoptera). J Nat Hist 31:1127–1141

    Article  Google Scholar 

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

    Article  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

    Article  CAS  Google Scholar 

  • Fonseca PJ, Münch D, Hennig RM (2000) How cicadas interpret acoustic signals. Nature 405:297–298

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  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 22:26–28

    Article  Google Scholar 

  • Göpfert MC, Wasserthal LT (1999) Auditory sensory cells in hawkmoths: identification, physiology and structure. J Exp Biol 202:1579–1587

    PubMed  Google Scholar 

  • Göpfert MC, Surlykke A, Wasserthal LT (2002) Tympanal and atympanal ‘mouth-ears’ in hawkmoths (Sphingidae). Proc Roy Soc Lond B 269:89–95

    Article  Google Scholar 

  • Graber V (1881) Über die stiftführenden und chordotonalen Sinnesorgane bei den Insekten. Zool Anz 4:450–453

    Google Scholar 

  • Greenfield MD (2002) Signalers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, Oxford

    Google Scholar 

  • Grimaldi D, Engel MS (2005) Evolution of the insects. Cambridge University Press, Cambridge

    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

    Article  PubMed  CAS  Google Scholar 

  • Gwynne DT (2004) Reproductive behavior of ground weta (Orthoptera: Anostostomatidae): drumming behavior, nuptial feeding, post-copulatory guarding and maternal care. J Kansas Entomol Soc 77:414–428

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • Hoch H, Deckert J, Wessel A (2006) Vibrational signalling in a Gondwanan relict insect (Hemiptera: Coleorrhyncha: Peloridiidae). Biol Lett 2:222–224

    Article  PubMed  Google Scholar 

  • Hoy RR (1992) The evolution of hearing in insects as an adaptation to predation from bats. In: Webster D, Fay R, Popper A (eds) Comparative and evolutionary biology of hearing. Springer, New York, pp 115–130

    Chapter  Google Scholar 

  • Hoy RR, Robert D (1996) Tympanal hearing in insects. Ann Rev Entomol 41:433–445

    Article  CAS  Google Scholar 

  • Jeram S, Rössler W, Cokl 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

    Article  Google Scholar 

  • Kalmring K, Kühne R (1980) The coding of airborne-sound and vibration signals in bimodal ventral-cord neurons of the grasshopper Tettigonia cantans. J Comp Physiol 139:267–275

    Article  Google Scholar 

  • Kalmring K, Rössler W, Unrast C (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 270:155–161

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kernan MJ (2007) Mechanotransduction and auditory transduction in Drosophila. Pflugers Arch Eur J Physiol 454:703–720

    Google Scholar 

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

    Article  Google Scholar 

  • Kutty SN, Pape Th, Wiegmann BM, Meier R (2010) Molecular phylogeny of the Calyptratae (Diptera: Cyclorrhapha) with an emphasis on the superfamily Oestroidea and the position of Mystacinobiidae and McAlpine’s fly. Syst Entomol 35:614–635

    Article  Google Scholar 

  • Lakes-Harlan R, Heller K-G (1992) Ultrasound-sensitive ears in a parasitoid fly. Naturwissenschaften 79:224–226

    Article  Google Scholar 

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

    Article  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

    Article  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

    Article  Google Scholar 

  • Lehmann GUC, Berger S, Strauß J, Lehmann AW, Pflüger HJ (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 

  • Legendre F, Robillard T, Song H, Whiting MF, Desutter-Grandcolas L (2010) One hundred years of instability in ensiferan relationships. Syst Entomol 35:475–488

    Article  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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Michel K (1979) Ein neuer Typ eines Grillenohres: Konstruktion und Ultrastruktur eines Tympanalorgans von Cycloptiloides canariensis (Bolivar) (Mogoplistinae, Gryllidae). Zool Anzeiger 203:139–150

    Google Scholar 

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

    Article  Google Scholar 

  • Moiseff A, Pollack GS, Hoy RR (1978) Steering responses of flying crickets to sound and ultrasound: mate attraction and predator avoidance. Proc Natl Acad Sci USA 75:4052–4056

    Article  PubMed  CAS  Google Scholar 

  • Moulins M (1976) Ultrastructure of chordotonal organs. In: Mill PJ (ed) Structure and function of proprioceptors in the invertebrates. Chapman and Hall, London, pp 387–426

    Google Scholar 

  • Nocke N (1975) Physical and physiological properties of the tettigoniid (‘grasshopper’) ear. J Comp Physiol 100:25–57

    Article  Google Scholar 

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

    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 

  • Plotnick RE, Smith DM (2012) Exceptionally preserved fossil insect ears from the Eocene Green River formation of Colorado. J Paleontol 86:19–24

    Article  Google Scholar 

  • Pollack GS (2000) Who what where? Recognition and localization of acoustic signals by insects. Curr Opin Neurobiol 10:763–767

    Article  PubMed  CAS  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

    Article  PubMed  Google Scholar 

  • Prager J (1976) Das mesothorakale Tympanalorgan von Corixa punctata Ill. (Heteroptera, Corixidae). J Comp Physiol 110:33–50

    Google Scholar 

  • Radl E (1905) Über das Gehör der Insekten. Biol Centralblatt 25:1–5

    Google Scholar 

  • Regier JC, Zwick A, Cummings MP, Kawahara AY, Cho S, Weller S, Roe A, Baixeras J, Brown JW, Parr C, Davis DR, Epstein M, Hallwachs W, Hausmann A, Janzen DH, Kitching IJ, Solis M, Yen S-H, Bazinet AL, Mitter C (2009) Towards reconstructing the evolution of advanced moths and butterflies (Lepidoptera: Ditrysia): an initial molecular study. BMC Evol Biol 9:280

    Article  PubMed  Google Scholar 

  • Riede K (1987) A comparative study of mating behaviour in some neotropical grasshoppers (Acridoidea). Ethology 76:265–296

    Article  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

    Article  Google Scholar 

  • Roeder KD (1967) Nerve cells and insect behavior. Harvard University Press, Cambridge

    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

    Article  Google Scholar 

  • Rust J, Gottwald J, Stumpner A (1999) Singing and hearing in a Tertiary bushcricket. Nature 399:650

    Article  CAS  Google Scholar 

  • Schäffer S, Lakes-Harlan R (2001) Embryonic development of the central projection of auditory afferents (Schistocerca gregaria, Orthoptera, Insecta). J Neurobiol 46:97–112

    Google Scholar 

  • Schumacher R (1979) Zur funktionellen Morphologie des auditiven Systems der Laubheuschrecken (Orthoptera: Tettigonioidea). Entomol Generalis 5:321–356

    Google Scholar 

  • Shaw SR (1994) Re-evaluation of the absolute threshold and response mode of the most sensitive know vibration detector, the cockroach’s subgenual organ: a cochlea-like displacement threshold and a direct response to sound. J Neurobiol 25:1167–1185

    Article  PubMed  CAS  Google Scholar 

  • Simmons NB, Seymour KL, Habersetzer J, Gunnell GF (2008) Primitive early Eocene bat from Wyoming and the evolution of flight and echolocation. Nature 451:818–821

    Article  PubMed  CAS  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

    Article  PubMed  Google Scholar 

  • Strauß J, Lakes-Harlan R (2008a) 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

    Article  PubMed  Google Scholar 

  • Strauß J, Lakes-Harlan R (2008b) Neuroanatomy of the complex tibial organ of Stenopelmatus (Orthoptera: Ensifera: Stenopelmatidae). J Comp Neurol 511:81–91

    Article  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

    Article  PubMed  Google Scholar 

  • Strauß J, Lakes-Harlan R (2010) Neuroanatomy of the complex tibial organ of the splay-footed cricket, Comicus calcaris (Orthoptera: Ensifera: Schizodactylidae). J Comp Neurol 518:4567–4580

    Article  PubMed  Google Scholar 

  • Strauß J, Lehmann GUC, Lehmann AW, Lakes-Harlan R (2012) Spatial organization of tettigoniid auditory receptors: insights from neuronal tracing. J Morphol 273:1280–1290

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Surlykke A (1984) Hearing in notodontid moths: a tympanic organ with a single auditory neuron. J Exp Biol 113:323–335

    Google Scholar 

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

    Article  Google Scholar 

  • Webster DB, Fay RR, Popper AN (1992) Comparative and evolutionary biology of hearing. Springer, New York

    Book  Google Scholar 

  • Weissman DB (2001) Communication and reproductive behaviour in North American Jerusalem crickets (Stenopelmatus) (Orthoptera: Stenopelmatidae). In: Field L (ed) The biology of wetas, king crickets and their allies. CABI Publishing, Wallingford, pp 351–373

    Chapter  Google Scholar 

  • Wheeler WC, Whiting M, Wheeler QD, Carpenter JM (2001) The phylogeny of the extant hexapod orders. Cladistics 17:113–169

    Article  Google Scholar 

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

    Article  PubMed  CAS  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 300:523–534

    Article  PubMed  CAS  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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yack JE, Hoy RR (2003) Hearing. In: Resh VH, Carde RT (eds) Encyclopedia of insects. Academic Press, San Diego, pp 498–505

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yager DD, Spangler HG (1995) Characterization of auditory afferents in the tiger beetle, Cicindela marutha Dow. J comp Physiol A 176:587–599

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. AG Integrative Sensory Physiology, Institute for Animal Physiology, Justus-Liebig-Universität Gießen, Heinrich-Buff-Ring 26, 35392, Gießen, Germany

    Johannes Strauß & Reinhard Lakes-Harlan

Authors
  1. Johannes Strauß
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Reinhard Lakes-Harlan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Johannes Strauß .

Editor information

Editors and Affiliations

  1. Department of Zoology, University of Cambridge, Cambridge, United Kingdom

    Berthold Hedwig

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Strauß, J., Lakes-Harlan, R. (2014). Evolutionary and Phylogenetic Origins of Tympanal Hearing Organs in Insects. In: Hedwig, B. (eds) Insect Hearing and Acoustic Communication. Animal Signals and Communication, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-40462-7_2

Download citation

Publish with us

Policies and ethics

Search

Navigation