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.

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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.

Notes

  1. 1.

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

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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.

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Correspondence to Tigga Kingston.

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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)

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

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