Convergent evolution of anti-bat sounds

Abstract

Bats and their insect prey rely on acoustic sensing in predator prey encounters—echolocation in bats, tympanic hearing in moths. Some insects also emit sounds for bat defense. Here, we describe a previously unknown sound-producing organ in Geometrid moths—a prothoracic tymbal in the orange beggar moth (Eubaphe unicolor) that generates bursts of ultrasonic clicks in response to tactile stimulation and playback of a bat echolocation attack sequence. Using scanning electron microscopy and high-speed videography, we demonstrate that E. unicolor and phylogenetically distant tiger moths have evolved serially homologous thoracic tymbal organs with fundamentally similar functional morphology, a striking example of convergent evolution. We compared E. unicolor clicks to that of five sympatric tiger moths and found that 9 of 13 E. unicolor clicking parameters were within the range of sympatric tiger moths. Remaining differences may result from the small size of the E. unicolor tymbal. Four of the five sympatric clicking tiger moth species were unpalatable to bats (0–20 % eaten), whereas E. unicolor was palatable to bats (86 % eaten). Based on these results, we hypothesize that E. unicolor evolved tymbal organs that mimic the sounds produced by toxic tiger moths when attacked by echolocating bats.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Barber JR, Conner WE (2006) Tiger moth responses to a simulated bat attack: timing and duty cycle. J Exp Biol 209:2637–2650

    CAS  PubMed  Article  Google Scholar 

  2. Barber JR, Conner WE (2007) Acoustic mimicry in a predator–prey interaction. Proc Natl Acad Sci USA 104:9331

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  3. Barber JR, Kawahara AY (2013) Hawkmoths produce anti-bat ultrasound. Biol Lett 9. doi:10.1098/rsbl.2013.0161

  4. Barber JR, Chadwell BA, Garrett N, Schmidt-French B, Conner WE (2009) Naïve bats discriminate arctiid moth warning sounds but generalize their aposematic meaning. J Exp Biol 212:2141–2148

    PubMed  Article  Google Scholar 

  5. Bates DL, Fenton MB (1990) Aposematism or startle? Predators learn their responses to the defenses of prey. Can J Zool 68:49–52

    Article  Google Scholar 

  6. Blest AD, Collett TS, Pye JD (1963) The generation of ultrasonic signals by a new world arctiid moth. Proc R Soc Lond B 158:196–207

    Article  Google Scholar 

  7. Bura VL, Fleming AJ, Yack JE (2009) What’s the buzz? Ultrasonic and sonic warning signals in caterpillars of the great peacock moth (Saturnia pyri). Naturwissenschaften 96(713):718

    Google Scholar 

  8. Clare EL, Symondson WOC, Fenton MB (2014) An inordinate fondness for beetles? Variation in seasonal dietary preferences of night roosting big brown bats (Eptesicus fuscus). Mol Ecol. doi:10.1111/mec.12519 (In Press)

    Google Scholar 

  9. Conner WE (1999) ‘Un chant d’appel amoureux’: acoustic communication in moths. J Exp Biol 202:1711–1723

    PubMed  Google Scholar 

  10. 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  Article  Google Scholar 

  11. Corcoran AJ, Conner WE (2012) Sonar jamming in the field: effectiveness and behavior of a unique prey defense. J Exp Biol 215:4278–4287

    PubMed  Article  Google Scholar 

  12. Corcoran AJ, Barber JR, Conner WE (2009) Tiger moth jams bat sonar. Science 325:325–327

    CAS  PubMed  Article  Google Scholar 

  13. Corcoran AJ, Conner WE, Barber JR (2010) Anti-bat tiger moth sounds: form and function. Curr Zool 56:358–369

    Google Scholar 

  14. Corcoran AJ, Barber JR, Hristov NI, Conner WE (2011) How do tiger moths jam bat sonar? J Exp Biol 214:2416–2425

    PubMed  Article  Google Scholar 

  15. Corcoran AJ, Wagner RD, Conner WE (2013) Optimal predator risk assessment by the sonar-jamming arctiine moth Bertholdia trigona. PLoS One 8:e63609

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  16. Dunning DC (1968) Warning sounds of moths. Zeitschrift Fur Tierpsychologie 25:129–138

    CAS  PubMed  Google Scholar 

  17. Fullard J, Heller B (1990) Functional organization of the arctiid moth tymbal (Insecta, Lepidoptera). J Morphol 204:57–65

    Article  Google Scholar 

  18. Fullard JH, Fenton MB, Simmons JH (1979) Jamming bat echolocation: the clicks of arctiid moths. Can J Zool 57:647–649

    Article  Google Scholar 

  19. Gopfert MC, Wasserthal LT (1999) Hearing with the mouthparts: behavioral responses and the structural basis of ultrasound perception in acherontiine hawkmoths. J Exp Biol 202:909–918

    PubMed  Google Scholar 

  20. Heller KG, Achmann R (1993) The ultrasonic song of the moth Amyna natalis (Lepidoptera: acontiinae). Bioacoustics 5:89–97

    Article  Google Scholar 

  21. Hristov NI, Conner WE (2005a) Sound strategy: acoustic aposematism in the bat–tiger moth arms race. Naturwissenschaften 92:164–169

    CAS  PubMed  Article  Google Scholar 

  22. Hristov NI, Conner WE (2005b) Effectiveness of tiger moth (Lepidoptera, Arctiidae) chemical defenses against an insectivorous bat (Eptesicus fuscus). Chemoecology 15:105–113

    Article  Google Scholar 

  23. Jones G, Holderied MW (2007) Bat echolocation calls: adaptation and convergent evolution. Proc R Soc B 274:905–912

    PubMed Central  PubMed  Article  Google Scholar 

  24. Jones G, Teeling EC (2006) The evolution of echolocation in bats. Trends Ecol Evol 21:149–156

    PubMed  Article  Google Scholar 

  25. Linsley EG, Eisner T, Klots AB (1961) Mimetic assemblages of sibling species of lycid beetles. Evolution 15:15–29

    Article  Google Scholar 

  26. Miller LA (1991) Arctiid moth clicks can degrade the accuracy of range difference discrimination in echolocating big brown bats, Eptesicus fuscus. J Comp Physiol A 168:571–579

    CAS  PubMed  Article  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. Mohl B, Miller LA (1976) Ultrasonic clicks produced by the peacock butterfly: a possible bat-repellent mechanism. J Exp Biol 64:639–644

    Google Scholar 

  29. Nakano R, Takanashi T, Fujii T, Skals N, Surlykke A, Ishikawa Y (2009) Moths are not silent, but whisper ultrasonic courtship songs. J Exp Biol 212:4072–4078

    CAS  PubMed  Article  Google Scholar 

  30. 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  Article  Google Scholar 

  31. Nakano R, Ihara F, Mishiro K, Toyama M (2012) Male courtship ultrasound produced by mesothoracic tymbal organs in the yellow peach moth Conogethes punctiferalis (Lepidoptera: Crambidae). Jpn J Appl Entomol Zool 47:129–135

    Google Scholar 

  32. Nakano R, Takanashi T, Surlykke A, Skals N, Ishikawa Y (2013) Evolution of deceptive and true courtship songs in moths. Sci Rep 3. doi:10.1038/srep02003

    Google Scholar 

  33. Ratcliffe JM, Fullard JH (2005) The adaptive function of tiger moth clicks against echolocating bats: an experimental and synthetic approach. J Exp Biol 208:4689–4698

    PubMed  Article  Google Scholar 

  34. Ratcliffe JM, Nydam ML (2008) Multimodal warning signals for a multiple predator world. Nature 455:96–99

    CAS  PubMed  Article  Google Scholar 

  35. Skals N, Surlykke A (1999) Sound production by abdominal tymbal organs in two moth species: the green silver-line and the scarce silver line (Noctuoidea: Nolidae: Chloephorinae). J Exp Biol 202:2937–2949

    PubMed  Google Scholar 

  36. Spangler HG (1986) Functional and temporal analysis of sound production in Galleria mellonella L. (Lepidoptera: Pyralidae). J Comp Physiol A 159:751–756

    Article  Google Scholar 

  37. Spangler HG (1988) Moth hearing, defense, and communication. Ann Rev Entomol 33:59–81

    Article  Google Scholar 

  38. Stapells DR, Picton TW, Smith AD (1982) Normal hearing thresholds for clicks. J Acoust Soc Am 72:74–79

    CAS  PubMed  Article  Google Scholar 

  39. Tougaard J, Casseday J, Covey E (1998) Arctiid moths and bat echolocation: broad-band clicks interfere with neural responses to auditory stimuli in the nuclei of the lateral lemniscus of the big brown bat. J Comp Physiol A 182:203–215

    CAS  PubMed  Article  Google Scholar 

  40. Yack JE, Dawson JW (2008) Insect ears. In: Hoy RR, Sheperd GM, Basbaum A, Kaneko A (eds) The senses: a comprehensive reference, vol 3. Academic Press, Oxford, pp 35–54

    Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  43. Yager DD, Spangler HG (1997) Behavioral response to ultrasound by the tiger beetle Cicendela marutha Dow combines aerodynamic changes and sound production. J Exp Biol 200:649–659

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the staff of the Southwestern Research Station for coordination of field research, and Nick Dowdy for field assistance. William Conner and Gerald Carter reviewed a former version of this manuscript. Funding was provided by the National Science Foundation (Grant Number IOS-0951160), the American Museum of Natural History (Theodore Roosevelt Grant) and by an institutional training grant (UMD T32 DC-00046) from the National Institute of Deafness and Communicative Disorders of the National Institutes of Health. All research on vertebrates was approved by the Wake Forest University Animal Care and Use Committee (IACUC #A09-094).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Aaron J. Corcoran.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Resource 1. High-speed video of the tymbal of the geometrid moth Eubaphe unicolor. Audio and video are slowed 30x. Image is shown with anterior toward the bottom of the image and dorsal toward the right of the image. Note the faintly visible striae on the posterior edge of the tymbal

Supplementary material 1 (MPG 2374 kb)

Online Resource 2. High-speed video of the tymbal of the arctiine moth Cycnia tenera. Audio and video are slowed 30x. Image is shown with anterior toward the top-left of the image and dorsal toward the top-right of the image. Note the faintly visible striae on the anterior edge of the tymbal

Supplementary material 2 (MPG 4158 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Corcoran, A.J., Hristov, N.I. Convergent evolution of anti-bat sounds. J Comp Physiol A 200, 811–821 (2014). https://doi.org/10.1007/s00359-014-0924-0

Download citation

Keywords

  • Batesian mimicry
  • Bioacoustics
  • Predator defense
  • Sound production
  • Tymbal organ