Parasitoid flies exploiting acoustic communication of insects—comparative aspects of independent functional adaptations

Journal of Comparative Physiology A: Neuroethology, Sensory, Neural, and Behavioral Physiology

Volumn 201, Issue 1, 2015, Pages 123-132

  Lakes Harlan, Reinhard ^a   Lehmann, Gerlind U C ^b  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Frequency tuning; Hearing; Host localization; Host range; Signal evolution

Indexed keywords

ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL COMMUNICATION; DIPTERA; EVOLUTION; HEARING; HOST PARASITE INTERACTION; PHYSIOLOGY;

ANIMAL COMMUNICATION; ANIMALS; BIOLOGICAL EVOLUTION; DIPTERA; HEARING; HOST-PARASITE INTERACTIONS;

EID: 84920461361     PISSN: 03407594     EISSN: 14321351     Source Type: Journal    
DOI: 10.1007/s00359-014-0958-3     Document Type: Review

References (68)

1. Adamo SA, Robert D, Perez J, Hoy RR (1995) The response of an insect parasitoid, Ormia ochracea (Tachinidae), to the uncertainty of larval success during infestation. Behav Ecol Sociobiol 36:111–118
2. Allen GR, Hunt J (2001) Larval competition, adult fitness and reproductive strategies in the acoustically-orienting ormiine Homotrixa alleni (Diptera: Tachinidae). J Ins Behav 14:283–297
3. Allen GR, Kamien D, Berry O, Byrne P, Hunt J (1999) Larviposition, host cues, and planidial behavior in the sound-locating parasitoid fly Homotrixa alleni (Diptera: Tachinidae). J Ins Behav 12:67–79
4. Arthur B, Hoy R (2006) The ability of the parasitoid fly Ormia ochracea to distinguish sounds in the vertical plane. J Acoust Soc Am 120:1546–1549
5. Bailey WJ (1991) Acoustic behaviour of insects. An evolutionary perspective. Chapman and Hall, London
6. 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
7. Bailey N, Zuk M (2008) Acoustic experience shapes female mate choice in field crickets. Proc Roy Soc Biol Sci 275:2645–2650
8. Boulard M (2006) Acoustic signals, diversity and behaviour of cicadas (Cicadidae, Hemiptera). In: Drosopoulos S, Claridge MF (eds) Insect sound and communication. CRC Press, Boca Raton, pp 331–349
9. deVries T, Lakes-Harlan R (2005) Phonotaxis of Emblemasoma auditrix (Sarcophagidae, Diptera) in relation to number of larvae and age. Zoology 108:239–246
10. Edgecomb RS, Robert D, Read MP, Hoy RR (1995) The tympanal hearing organ of a fly: phylogenetic analysis of its morphological origin. Cell Tiss Res 282:251–268
11. Farris HE, Oshinsky ML, Forrest TG, Hoy R (2008) Auditory sensitivity of an acoustic parasitoid (Emblemasoma sp., Sarcophagidae, Diptera) and the calling behavior of potential hosts. Brain Behav Evol 72:16–26
12. Fullard JH, Yack JE (1993) The evolutionary biology of insect hearing. Trends Ecol Evol 8:248–252
13. Gerhardt HC, Huber F (2002) Acoustic communication in insects and anurans: common problems and divers solutions. Chicago University Press, Chicago
14. Godfray H (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, New Jersey
15. Goles E, Schulz O, Markus M (2001) Prime number selection of cycles in a predator-prey model. Complexity 6:33–38
16. Gray DA, Banuelos C, Walker SS, Cade WH, Zuk M (2007) Behavioural specialization among populations of the acoustically orienting parasitoid fly Ormia ochracea utilizing different cricket species as hosts. Anim Behav 73:99–104
17. Greenfield M (2002) Signallers and receivers: mechanisms and evolution of arthropod communication. Oxford University Press, Oxford
18. Gwynne D, Bailey WJ (1999) Female–female competition on katydids: sexual selection for increased sensitivity to a male signal? Evolution 53:546–551
19. Hedwig B, Robert D (2014) Auditory parasitoid flies exploiting acoustic commuincation of insects. In: Hedwig B (ed) Insect hearing and acoustic communication. Animal signals and communication. Springer, New York, pp 45–65
20. Heller K-G (1988) Bioakustik der europäischen Laubheuschrecken. Margraf Verlag, Weikersheim
21. Heller K-G, Von Helversen O (1993) Calling behavior in bushcrickets of the genus Poecilimon with differing communication systems (Orthoptera: Tettigonioidea, Phaneropteridae). J Ins Behav 6:361–377
22. Köhler U, Lakes-Harlan R (2001) Auditory behaviour of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera). J Comp Physiol A 187:581–587
23. Lakes-Harlan R, Heller K-G (1992) Ultrasound-sensitive ears in a parasitoid fly. Naturwissenschaften 79:224–226
24. Lakes-Harlan R, Köhler U (2003) Influence of habitat structure on phonotactic strategy of a parasitoid fly (Emblemasoma auditrix, Sarcophagidae, Diptera). Ecol Entomol 28:758–765
25. Lakes-Harlan R, Stölting H, Stumpner A (1999) Convergent evolution of insect hearing organs from a preadaptive structure. Proc Roy Soc Biol Sci 266:1161–1167
26. Lakes-Harlan R, Stölting H, Moore TE (2000) Phonotactic behavior of a parasitoid (Emblemasoma auditrix, Sarcophagidae, Diptera) in response to the calling song of the host (Okanagana rimosa, Cicada, Homoptera). Zoology 103:31–39
27. Lakes-Harlan R, Jacobs K, Allen G (2007) Comparison of auditory sense organs in parasitoids Tachinidae (Diptera) hosted by Tettigoniidae (Orthoptera) and homologous structures in a non-hearing Phoridae (Diptera). Zoomorphology 126:229–243
28. 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:e87211
29. Lee N, Elias DO, Mason AC (2009) A precedence effect resolves phantom sound source illusions in the parasitoid fly Ormia ochracea. Proc Nat Acad Sci USA 106:6357–6362
30. Lehmann GUC (2003) Review of biogeography, host range and evolution of acoustic hunting in Ormiini (Insects, Diptera, Tachinidae), parasitoids of night-calling bushcrickets and crickets (Insecta, Orthoptera, Ensifera). Zool Anz 242:107–120
31. Lehmann GUC (2008) How different host species influence parasitism pattern and larval competition of acoustically-orienting parasitoid flies (Tachinidae: Ormiini). In: Krause L, Weber E (eds) Animal behavior: new research. Nova Science Publishers, New York, pp 93–132
32. Lehmann GUC, Heller K-G (1998) Bushcricket song structure and predation by the acoustically orienting parasitoid fly Therobia leonidei (Diptera: Tachinidae: Ormiini). Behav Ecol Sociobiol 43:239–245
33. Lehmann GUC, Lehmann AW (2000) Female bushcrickets mated with parasitized males show rapid remating and reduced fecundity (Orthoptera: Phaneropteridae: Poecilimon mariannae). Naturwissenschaften 87:404–407
34. Lehmann GUC, Lehmann AW (2006) Potential lifetime reproductive success of male bushcrickets parasitized by a phonotactic fly. Anim Behav 71:1103–1110
35. Lehmann GUC, Lehmann AW (2008) Bushcricket song as a clue for spermatophore size? Behav Ecol Sociobiol 62:569–578
36. Lehmann GUC, Heller K-G, Lehmann AW (2001) Male bushcrickets favoured by parasitoid flies when acoustically more attractive for conspecific females (Orthoptera: Phanopteridae/Diptera: Tachinidae). Entomol Gen 25:135–140
37. Mason AC, Oshinsky ML, Hoy RR (2001) Hyperacute directional hearing in a microscale auditory system. Nature 410:686–690
38. Mason AC, Lee N, Oshinsky ML (2005) The start of phonotactic walking in the fly Ormia ochracea: a kinematic study. J Exp Biol 208:4699–4708
39. Michelsen A (1992) Directional hearing in crickets and other small animals. In: Schildberger E, Elsner N (eds) Neural basis of behavioural adaptations, vol 19. Fortschritte der Biologie. pp 195–207
40. Miles RN, Robert D, Hoy RR (1995) Mechanically coupled ears for directional hearing in the parasitoid fly Ormia ochracea. J Acoust Soc Am 98:3059–3070
41. Müller P, Robert D (2001) A shot in the dark: the silent quest of a free-flying phonotactic fly. J Exp Biol 204:1039–1052
42. Oshinsky ML, Hoy RR (2002) Physiology of the auditory afferents in an acoustic parasitoid fly. J Neurosci 22:7254–7263
43. Pascoal S, Cezard T, Eik-Nes A, Gharbi K, Majewska J, Payne E, Ritchie MG, Zuk M, Bailey NW (2014) Rapid convergent evolution in wild crickets. Curr Biol 24:1369–1374
44. Ramsauer N, Robert D (2000) Free-flight phonotaxis in a parasitoid fly: behavioural thresholds, relative attraction and susceptibility to noise. Naturwissenschaften 87:315–319
45. Robert D, Willi D (2000) The histological architecture of the auditory organs in the parasitoid fly Ormia ochracea. Cell Tiss Res 301:447–457
46. Robert D, Amoroso J, Hoy RR (1992) The evolutionary convergence of hearing in a parasitoid fly and its cricket host. Science 258:1135–1137
47. Robert D, Edgecomb RS, Read MP, Hoy RR (1996a) Tympanal hearing in tachinid flies (Diptera, Tachinidae, Ormiini): the comparative morphology of an innovation. Cell Tiss Res 284:435–448
48. Robert D, Miles RN, Hoy RR (1996b) Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea. J Comp Physiol A 179:29–44
49. Robert D, Miles R, Hoy RR (1998) Tympanal mechanics in the parasitoid fly Ormia ochracea: intertympanal coupling during mechanical vibration. J Comp Physiol A 183:443–452
50. Robert D, Miles RN, Hoy RR (1999) Tympanal hearing in the sarcophagid parasitoid fly Emblemasoma sp.: the biomechanics of directional hearing. J Exp Biol 202:1865–1876
51. Römer H (1987) Representation of auditory distance within a central neuropil of the bushcricket Mygalopsis marki. J Comp Physiol A 161:33–42
52. Römer H, Bailey W (1998) Strategies for hearing in noise: peripheral control over auditory sensitivity in the bushcricket Sciarasaga quadrata (Austrosaginae: Tettigoniidae). J Exp Biol 201:1023–1033
53. Rosen MJ, Levin EG, Hoy RR (2009) The cost of assuming life history of a host: acoustic startle in the parasitoid fly Ormia ochracea. J Exp Biol 212:4056–4064
54. Schniederkötter K, Lakes-Harlan R (2004) Infection behavior of a parasitoid fly, Emblemasoma auditrix and its host cicada Okanagana rimosa. J Ins Sci 4:36–37
55. Stölting H (2000) Morphologie und Physiologie der tympanalen auditorischen Systeme und des evolutionären Vorläuferorgans bei Fliegen. Dissertation, University Göttingen
56. Stölting H, Moore TA, Lakes-Harlan R (2004) Acoustic communication of Okanagana rimosa (Say) (Homoptera: Cicadidae). Zoology 107:243–257
57. 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
58. 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. Animal signals and communication. Springer, New York, pp 5–26
59. Stumpner A, Lakes-Harlan R (1996) Auditory interneurons in a hearing fly (Therobia leonidei, Ormiini, Tachinidae, Diptera). J Comp Physiol A 178:227–233
60. Stumpner A, Allen G, Lakes-Harlan R (2007) Hearing and frequency dependence of auditory interneurons in the parasitoid fly Homotrixa alleni (Tachinidae: Ormiini). J Comp Physiol A 193:113–125
61. Walker TJ (1993) Phonotaxis in female Ormia ochracea (Diptera: Tachinidae), a parasitoid of field crickets. J Ins Behav 6:389–410
62. Walker TJ, Wineriter A (1991) Hosts of a phonotactic parasitoid and levels of parasitism (Diptera: Tachinidae: Ormia ochracea). Fla Ent 74:554–559
63. Williams KS, Simon C (1995) The ecology, behavior, and evolution of periodical cicadas. Annu Rev Entomol 40:269–295
64. Yager DD (1999) Structure, development, and evolution of insect auditory systems. Microsc Res Tech 47:380–400
65. Zuk M, Kolluru GR (1998) Exploitation of sexual signals by predators and parasitoids. Quart Rev Biol 73:415–438
66. Zuk M, Simmons LW, Cupp L (1993) Calling characteristics of parasitized and unparasitized populations of the field cricket Teleogryllus oceanicus. Behav Ecol Sociobiol 33:339–343
67. Zuk M, Simmons LW, Rotenberry JT (1995) Acoustically-orienting parasitoids in calling and silent males of the field cricket Teleogryllus oceanicus. Ecol Entomol 20:380–383
68. 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