, 97:53 | Cite as

Release from bats: genetic distance and sensoribehavioural regression in the Pacific field cricket, Teleogryllus oceanicus

  • James H. FullardEmail author
  • Hannah M. ter Hofstede
  • John M. Ratcliffe
  • Gerald S. Pollack
  • Gian S. Brigidi
  • Robin M. Tinghitella
  • Marlene Zuk


The auditory thresholds of the AN2 interneuron and the behavioural thresholds of the anti-bat flight-steering responses that this cell evokes are less sensitive in female Pacific field crickets that live where bats have never existed (Moorea) compared with individuals subjected to intense levels of bat predation (Australia). In contrast, the sensitivity of the auditory interneuron, ON1 which participates in the processing of both social signals and bat calls, and the thresholds for flight orientation to a model of the calling song of male crickets show few differences between the two populations. Genetic analyses confirm that the two populations are significantly distinct, and we conclude that the absence of bats has caused partial regression in the nervous control of a defensive behaviour in this insect. This study represents the first examination of natural evolutionary regression in the neural basis of a behaviour along a selection gradient within a single species.


Neuroethology Genetic isolation Evolution Sensory ecology Island biology 



For assistance while in the field, we thank Neil Davies and the staff of the Richard B. Gump South Pacific Research Station (Moorea, Polynésie française), Gerald McCormack (Cook Islands Natural Heritage Project, Rarotonga, Cook Islands), and Chris R. Pavey (Department of Natural Resources, Environment and the Arts, Australia). We thank David Fang of the UC Riverside Genomics Center for assistance with the microsatellite analysis and Cheryl Hayashi for laboratory space. We also thank Michelle Venance, Steve Fynk, Millie Engel, Shannon Venance, and Maura Purdon for their field proficiency at cricket collecting. This work was supported by the Natural Sciences and Engineering Research Council of Canada Discovery Grants to J.H.F and G.S.P., a Journal of Experimental Biology Traveling Fellowship to H. M. t. H., a National Science Foundation Grant Doctoral Dissertation Improvement Grant to R.M.T. and M.Z., and a University of California Pacific Rim Mini-Grant to R.M.T. Studies were carried out in accordance with permits issued by the Délégation à la Recherche (Polynésie française), the Cook Islands Foundation for National Research (Cook Islands), and the Department of the Environment and Heritage and Northern Territory Parks and Wildlife (Australia).

Supplementary material

114_2009_610_MOESM1_ESM.doc (25 kb)
ESM S1 (DOC 25 kb)
114_2009_610_MOESM2_ESM.doc (26 kb)
ESM S2 (DOC 26 kb)
114_2009_610_MOESM3_ESM.doc (24 kb)
ESM S3 (DOC 24 kb)
114_2009_610_MOESM4_ESM.doc (25 kb)
ESM S4 (DOC 25 kb)
114_2009_610_MOESM5_ESM.doc (38 kb)
ESM S5 (DOC 38 kb)


  1. Balakrishnan R, Pollack GS (1996) Recognition of courtship song in the field cricket, Teleogryllus oceanicus. Anim Behav 51:353–366CrossRefGoogle Scholar
  2. Beveridge M, Simmons LW (2005) Microsatellite loci for the Australian field cricket Teleogryllus oceanicus and their cross-utility in Teleogryllus commodus. Mol Ecol Notes 5:733–735CrossRefGoogle Scholar
  3. Borowsky RB, Wilkens H (2002) Mapping a cave fish genome: polygenic systems and regressive evolution. J Heredity 93:19–21CrossRefGoogle Scholar
  4. Chopard L (1967) Gryllides. In: Beier M (ed) Orthopterorum Catalogus, Pars 10. Uitgevrij Dr W Junk, 's-Gravenhage, pp 1–211Google Scholar
  5. Churchill S (1998) Australian bats. New Holland, SydneyGoogle Scholar
  6. Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  7. Darwin C (1859) On the Origin of Species. John Murray, LondonGoogle Scholar
  8. Faulkes Z, Pollack GS (2000) Effects of inhibitory timing on contrast enhancement in auditory circuits in crickets (Teleogryllus oceanicus). J Neurophysiol 84:1247–1255PubMedGoogle Scholar
  9. Fong DW, Kane TC, Culver DC (1995) Vestigialization and loss of nonfunctional characters. Ann Rev Ecolog Syst 26:249–268CrossRefGoogle Scholar
  10. Fullard JH (1994) Auditory changes in noctuid moths endemic to a bat-free habitat. J Evol Biol 7:435–445CrossRefGoogle Scholar
  11. Fullard JH, Dawson JW, Otero LD, Surlykke A (1997) Bat-deafness in day-flying moths (Lepidoptera, Notodontidae, Dioptinae). J Comp Physiol A 181:477–483CrossRefPubMedGoogle Scholar
  12. Fullard JH, Ratcliffe JM, Soutar AR (2004) Extinction of the acoustic startle response in moths endemic to a bat-free habitat. J Evol Biol 17:856–861CrossRefPubMedGoogle Scholar
  13. Fullard JH, Ratcliffe JM, Guignion C (2005) Sensory ecology of predator–prey interactions: responses of the AN2 interneuron in the field cricket, Teleogryllus oceanicus to the echolocation calls of sympatric bats. J Comp Physiol A 191:605–618CrossRefGoogle Scholar
  14. 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 3:26–28CrossRefPubMedGoogle Scholar
  15. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Heredity 86:485–486Google Scholar
  16. Haldane JBS (1933) The part played by recurrent mutation in evolution. Am Nat 67:5–19CrossRefGoogle Scholar
  17. Harrison L, Horseman G, Lewis B (1988) The coding of the courtship song by an auditory interneurone in the cricket Teleogryllus oceanicus (Le Guillou). J Comp Physiol A 163:215–225CrossRefGoogle Scholar
  18. Hill KG, Loftus-Hills JJ, Gartside DF (1972) Premating isolation between the Australian field crickets Teleogryllus commodus and T. oceanicus (Orthoptera: Gryllidae). Aust J Zool 20:153–163CrossRefGoogle Scholar
  19. Hutchings M, Lewis B (1984) The role of two-tone suppression in song coding by ventral cord neurones in the cricket Teleogryllus oceanicus (Le Guillou). J Comp Physiol A 154:103–112CrossRefGoogle Scholar
  20. Kevan DKM (1990) Introduced grasshoppers and crickets in Micronesia. Bol Sanid Veg 20:105–123Google Scholar
  21. Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738PubMedGoogle Scholar
  22. Latimer W, Lewis DB (1986) Song harmonic content as a parameter determining acoustic orientation behaviour in the cricket Teleogryllus oceanicus (Le Guillou). J Comp Physiol A 158:583–591CrossRefGoogle Scholar
  23. Marsat G, Pollack GS (2006) A behavioral role for feature detection by sensory bursts. J Neurosci 26:10542–10547CrossRefPubMedGoogle Scholar
  24. Marsat G, Pollack GS (2007) Efficient inhibition of bursts by bursts in the auditory system of crickets. J Comp Physiol A 193:625–633CrossRefGoogle Scholar
  25. Mayr E (1942) Systematics and the origin of species. Columbia University Press, New YorkGoogle Scholar
  26. Miller LA, Surlykke A (2001) How some insects detect and avoid being eaten by bats: tactics and countertactics of prey and predator. Bioscience 51:570–581CrossRefGoogle Scholar
  27. Moiseff A, Hoy RR (1983) Sensitivity to ultrasound in an identified auditory interneuron in the cricket: a possible link to phonotactic behavior. J Comp Physiol 152:155–167CrossRefGoogle Scholar
  28. 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 75:4052–4056CrossRefPubMedGoogle Scholar
  29. Narbonne R, Pollack GS (2008) Developmental control of ultrasound sensitivity by a juvenile hormone analog in crickets (Teleogryllus oceanicus). J Insect Physiol 54:1552–1556CrossRefPubMedGoogle Scholar
  30. Nolen TG, Hoy RR (1984) Initiation of behavior by single neurons: the role of behavioral context. Science 226:992–994CrossRefPubMedGoogle Scholar
  31. Otte D, Alexander RD (1983) The Australian crickets (Orthoptera: Gryllidae). Academy of Natural Sciences of Philadelphia, PhiladelphiaGoogle Scholar
  32. Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. J Heredity 90:502–503CrossRefGoogle Scholar
  33. Pollack GS (1998) Neural processing of acoustic signals. In: Hoy RR, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, New York, pp 139–196Google Scholar
  34. Pollack GS, El-Feghaly E (1993) Calling song recognition in the cricket Teleogryllus oceanicus: comparison of the effects of stimulus intensity and sound spectrum on selectivity for temporal pattern. J Comp Physiol A 171:759–766CrossRefGoogle Scholar
  35. 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 210:3160–3164CrossRefPubMedGoogle Scholar
  36. Popov AV, Shuvalov VF (1977) Phonotactic behaviour of crickets. J Comp Physiol 119:111–126CrossRefGoogle Scholar
  37. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249Google Scholar
  38. Reznick DN, Ghalambor CK (2001) The population ecology of contemporary adaptation: what empirical studies reveal about the conditions that promote adaptive evolution. Genetica 112–113:183–198CrossRefPubMedGoogle Scholar
  39. Romero A, Green SM (2005) The end of regressive evolution: examining and interpreting the evidence from cave fishes. J Fish Biol 67:3–32CrossRefGoogle Scholar
  40. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792CrossRefPubMedGoogle Scholar
  41. Strausfeld NJ, Seyan HS, Wohlers D, Bacon JP (1983) Lucifer yellow histology. In: Strausfeld NJ (ed) Functional neuroanatomy. Springer-Verlag, Berlin, pp 132–155Google Scholar
  42. Surlykke A, Skals N, Rydell J, Svensson M (1998) Sonic hearing in a diurnal geometrid moth, Archiearis parthenias, temporally isolated from bats. Naturwissenschaften 85:36–37CrossRefGoogle Scholar
  43. Tinghitella RM (2008) Rapid evolutionary change in a sexual signal: genetic control of the mutation ‘flatwing’ that renders male field crickets (Teleogryllus oceanicus) mute. Heredity 100:261–267CrossRefPubMedGoogle Scholar
  44. van Dyck SM, Strahan R (2008) The mammals of Australia, 3rd edn. Reed New Holland, SydneyGoogle Scholar
  45. Vestjens WJM, Hall LS (1977) Stomach contents of forty-two species of bats from the Australasian region. Aust Wildl Res 4:25–35CrossRefGoogle Scholar
  46. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  47. Yager DD (1990) Sexual dimorphism of auditory function and structure in preying mantises (Mantodea; Dictyoptera). J Zool (Lond) 221:517–37CrossRefGoogle Scholar
  48. Yager DD (1999) Structure, development, and evolution of insect auditory systems. Microsc Res Tech 47:380–400CrossRefPubMedGoogle Scholar
  49. Zuk M, Rotenberry JT, Simmons LW (2001) Geographical variation in calling song of the field cricket Teleogryllus oceanicus: the importance of spatial scale. J Evol Biol 14:731–741CrossRefGoogle Scholar
  50. Zuk M, Rotenberry JT, Tinghitella RM (2006) Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biol Lett 2:521–524CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • James H. Fullard
    • 1
    Email author
  • Hannah M. ter Hofstede
    • 1
    • 5
  • John M. Ratcliffe
    • 2
  • Gerald S. Pollack
    • 3
  • Gian S. Brigidi
    • 3
  • Robin M. Tinghitella
    • 4
    • 6
  • Marlene Zuk
    • 4
  1. 1.Department of BiologyUniversity of Toronto MississaugaMississaugaCanada
  2. 2.Center for Sound Communication, Institute of BiologyUniversity of Southern DenmarkOdense MDenmark
  3. 3.Department of BiologyMcGill UniversityMontrealCanada
  4. 4.Department of BiologyUniversity of California-RiversideRiversideUSA
  5. 5.School of Biological SciencesUniversity of BristolBristolUK
  6. 6.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA

Personalised recommendations