Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Harmonic-hopping in Wallacea's bats

Abstract

Evolutionary divergence between species is facilitated by ecological shifts, and divergence is particularly rapid when such shifts also promote assortative mating1,2,3. Horseshoe bats are a diverse Old World family (Rhinolophidae) that have undergone a rapid radiation in the past 5 million years4. These insectivorous bats use a predominantly pure-tone echolocation call matched to an auditory fovea (an over-representation of the pure-tone frequency in the cochlea and inferior colliculus5,6) to detect the minute changes in echo amplitude and frequency generated when an insect flutters its wings7. The emitted signal is the accentuated second harmonic of a series in which the fundamental and remaining harmonics are filtered out8. Here we show that three distinct, sympatric size morphs of the large-eared horseshoe bat (Rhinolophus philippinensis) echolocate at different harmonics of the same fundamental frequency. These morphs have undergone recent genetic divergence, and this process has occurred in parallel more than once9. We suggest that switching harmonics creates a discontinuity in the bats' perception of available prey that can initiate disruptive selection1. Moreover, because call frequency in horseshoe bats has a dual function in resource acquisition and communication, ecological selection on frequency might lead to assortative mating and ultimately reproductive isolation and speciation, regardless of external barriers to gene flow1,2,3.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Relationship between constant-frequency component of calls and forearm length for three sympatric morphs of the large-eared horseshoe bat.
Figure 2: Echolocation calls of the three sympatric morphs of the large-eared horseshoe bat.
Figure 3: Consensus tree based on parsimony analysis of mtDNA haplotypes, showing phylogenetic relationships between large-eared horseshoe bat morphs sampled on Buton Island, Sulawesi, and Queensland, Australia.

Similar content being viewed by others

Notes

  1. Accession numbers for new and published sequences are AY568637–AY568646, and AF065069–AF065073 and AF065090 (ref. 12), respectively.

References

  1. Schluter, D. Ecology and the origin of species. Trends Ecol. Evol. 16, 372–380 (2001)

    Article  CAS  Google Scholar 

  2. Via, S. Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol. Evol. 16, 381–390 (2001)

    Article  CAS  Google Scholar 

  3. Rice, W. R. & Hostert, E. E. Perspective: Laboratory experiments on speciation: what have we learned in forty years? Evolution 47, 1637–1653 (1993)

    Article  Google Scholar 

  4. Guillén Servent, A., Francis, C. M. & Ricklefs, R. E. in Horseshoe Bats of the World (Chiroptera: Rhinolophidae) (eds Csorba, G., Ujhelyi, P. & Thomas, N) xii–xxiv (Alana Books, Bishop's Castle, Shropshire, UK, 2003)

    Google Scholar 

  5. Bruns, V. Peripheral auditory tuning for fine frequency analysis by the CF-FM bat, Rhinolophus ferrumequinum. I. Mechanical specializations of the cochlea. J. Comp. Physiol. 106, 77–86 (1976)

    Article  Google Scholar 

  6. Schuller, G. & Pollak, G. D. Disproportionate frequency representation in the inferior colliculus of Doppler-compensating greater horseshoe bats, evidence for an acoustic fovea. J. Comp. Physiol. A 132, 47–52 (1979)

    Article  Google Scholar 

  7. Schnitzler, H.-U. in Recent Advances in the Study of Bats (eds Fenton, M. B., Racey, P. A. & Rayner, J. M. V.) 226–243 (Cambridge Univ. Press, 1987)

    Google Scholar 

  8. Hartley, D. J. & Suthers, R. A. The acoustics of the vocal tract in the horseshoe bat, Rhinolophus hildebrandti. J. Acoust. Soc. Am. 84, 1201–1213 (1988)

    Article  ADS  Google Scholar 

  9. Schluter, D. & Nagel, L. M. Parallel speciation by natural selection. Am. Nat. 146, 292–301 (1995)

    Article  Google Scholar 

  10. Simmons, N. B. in Mammal Species of the World: A Taxonomic and Geographic Reference (eds Wilson, D. E. & Reeder, D. M.) 3rd edn (Smithsonian Institution Press, Washington DC, in the press)

  11. Cooper, S. J. B., Reardon, T. B. & Skilins, J. Molecular systematics of Australian rhinolophid bats (Chiroptera: Rhinolophidae). Aust. J. Zool. 46, 203–220 (1998)

    Article  Google Scholar 

  12. Pye, J. D. Is fidelity futile? The ‘true’ signal is illusory, especially with ultrasound. Bioacoustics 4, 271–286 (1993)

    Article  Google Scholar 

  13. Kober, R. & Schnitzler, H.-U. Information in sonar echoes of fluttering insects available for echolocating bats. J. Acoust. Soc. Am. 87, 882–896 (1990)

    Article  ADS  Google Scholar 

  14. Houston, R. D., Boonman, A. M. & Jones, G. in Echolocation in Bats and Dolphins (eds Thomas, J. A., Moss, C. F. & Vater, M.) 339–344 (Univ. of Chicago Press, 2004)

    Google Scholar 

  15. Lawrence, B. D. & Simmons, J. A. Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats. J. Acoust. Soc. Am. 71, 585–590 (1982)

    Article  CAS  ADS  Google Scholar 

  16. Jones, G. & Barlow, K. E. in Echolocation in Bats and Dolphins (eds Thomas, J. A., Moss, C. F. & Vater, M.) 345–349 (Univ. of Chicago Press, 2004)

    Google Scholar 

  17. NATO Advanced Study Institute & Möhres, F. P. Cours d'Été OTAN sur les Systèmes Sonars Animaux; Biologie et Bionique 2 939–945 (Laboratoire de Physiologie Acoustique, Paris, 1966)

    Google Scholar 

  18. Matsumura, S. Mother–infant communication in a horseshoe bat (Rhinolophus ferrumequinum nippon): vocal communication in three-week old infants. J. Mamm. 62, 20–28 (1981)

    Article  Google Scholar 

  19. Andrews, M. M. & Andrews, P. T. Ultrasound social calls made by greater horseshoe bats (Rhinolophus ferrumequinum) in a nursery roost. Acta Chiropterol. 5, 221–234 (2003)

    Article  Google Scholar 

  20. Long, G. R. & Schnitzler, H.-U. Behavioural audiograms from the bat, Rhinolophus ferrumequinum. J. Comp. Physiol. A 100, 211–219 (1975)

    Article  Google Scholar 

  21. Fenton, M. B. Communication in the Chiroptera (Indiana Univ. Press, 1985)

    Google Scholar 

  22. Francis, C. M. & Habersetzer, J. in Bat Biology and Conservation (eds Kunz, T. H. & Racey, P. A.) 169–181 (Smithsonian Institution Press, Washington DC, 1998)

    Google Scholar 

  23. Vater, M. in Ontogeny, Functional Ecology and Evolution of Bats (eds Adams, R. A. & Pedersen, S. C.) 137–173 (Cambridge Univ. Press, 2000)

    Book  Google Scholar 

  24. Rübsamen, R. & Schäfer, M. Audio-vocal interactions during development? Vocalisation in deafened young horseshoe bats vs. audition in vocalization-impaired bats. J. Comp. Physiol. A 167, 771–784 (1990)

    PubMed  Google Scholar 

  25. Rossiter, S. J., Burland, T. M., Jones, G. & Barratt, E. M. Characterization of microsatellite loci in the greater horseshoe bat Rhinolophus ferrumequinum. Mol. Ecol. 8, 1957–1969 (1999)

    Article  Google Scholar 

  26. Dawson, D. A., Rossiter, S. J., Jones, G. & Faulkes, C. F. Microsatellite loci for the greater horseshoe bat, Rhinolophus ferrumequinum (Rhinolophidae, Chiroptera) and their cross-utility in 17 other bat species. Mol. Ecol. Notes 4, 96–100 (2004)

    Article  CAS  Google Scholar 

  27. Nichols, R. A., Bruford, M. W. & Groombridge, J. J. Sustaining genetic variation in a small population: evidence from the Mauritius kestrel. Mol. Ecol. 10, 593–602 (2001)

    Article  CAS  Google Scholar 

  28. Stanley, H. F. et al. Worldwide patterns of mitochondrial DNA differentiation in the harbour seal (Phoca vitulina). Mol. Biol. Evol. 13, 368–382 (1996)

    Article  CAS  Google Scholar 

  29. Wilkinson, G. S. & Chapman, A. M. Length and sequence variation in Evening Bat D-Loop mtDNA. Genetics 128, 607–617 (1991)

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Churchill, S. Australian Bats (New Holland, Sydney, 1998)

    Google Scholar 

Download references

Acknowledgements

We thank the Indonesian Institute of Science (LIPI) and the Wallacea Development Institute for granting permissions to undertake this work, and T. Coles, Boeadi and Operation Wallacea staff and volunteers for logistical support in Indonesia. We thank Ririn and Samsudin for help in the field; A. Boonman, T. Burland, D. Dawson, C. Faulkes, K. Freeman, B. Kirsten, R. Nichols, L. Pettersson and J. Storz for advice on analysis and technical support; and B. Fenton and G. Jones for helpful comments on the manuscript. This work was funded by Operation Wallacea, and microsatellite development was supported by the NERC-funded Sheffield Molecular Genetics Facility.Authors’ contributions T.K. and S.J.R. performed the acoustic and genetic analyses, respectively, and jointly undertook the fieldwork and wrote the paper. The order of authors is alphabetical.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tigga Kingston.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Tables 1 and 2

Microsatellite allele frequencies for three sympatric size morphs of Rhinolophus philippinensis and two congeneric species, and pairwise mtDNA sequence divergence values among size morphs for Sulawesi and Australia. (DOC 258 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kingston, T., Rossiter, S. Harmonic-hopping in Wallacea's bats. Nature 429, 654–657 (2004). https://doi.org/10.1038/nature02487

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature02487

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing