Abstract

Urbanization can cause species to adjust their sexual displays, because the effectiveness of mating signals is influenced by environmental conditions. Despite many examples that show that mating signals in urban conditions differ from those in rural conditions, we do not know whether these differences provide a combined reproductive and survival benefit to the urban phenotype. Here we show that male túngara frogs have increased the conspicuousness of their calls, which is under strong sexual and natural selection by signal receivers, as an adaptive response to city life. The urban phenotype consequently attracts more females than the forest phenotype, while avoiding the costs that are imposed by eavesdropping bats and midges, which we show are rare in urban areas. Finally, we show in a translocation experiment that urban frogs can reduce risk of predation and parasitism when moved to the forest, but that forest frogs do not increase their sexual attractiveness when moved to the city. Our findings thus reveal that urbanization can rapidly drive adaptive signal change via changes in both natural and sexual selection pressures.

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Data availability

Raw data for the environmental samples, the translocation experiment and the female preference test can be found at the Dryad online depository (https://doi.org/10.5061/dryad.t78c588).

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Acknowledgements

We are grateful to L. de Herder, J. Smit and H. Loning for their help with collecting the data. We thank the Beta VU workshop for development of the playback devices and the Smithsonian Tropical Research Institute (STRI) for logistical support and in particular R. Taylor and K. Hunter for the use of the phonotaxis chamber. M. Still provided valuable advice on male and female sampling. The research was funded through a Marie Curie grant (655262), a Veni grant (863.15.006) and through the Ecology fund of the Royal Netherlands Academy of Arts and Sciences (713/18011). X.E.B. was funded by NSF grant IOS1433990.

Author information

Affiliations

  1. Department of Ecological Science, Vrije Universiteit, Amsterdam, The Netherlands

    • Wouter Halfwerk
    • , Michiel Blaas
    • , Lars Kramer
    • , Nadia Hijner
    •  & Jacintha Ellers
  2. Smithsonian Tropical Research Institute, Balboa, Republic of Panama

    • Wouter Halfwerk
    • , Paula A. Trillo
    • , Ximena E. Bernal
    • , Rachel A. Page
    •  & Michael J. Ryan
  3. Department of Biology, Gettysburg College, Gettysburg, PA, USA

    • Paula A. Trillo
  4. Department of Biological Sciences, Purdue University, West Lafayette, IN, USA

    • Ximena E. Bernal
  5. Department of Biology, University of New York at Abu Dhabi, Abu Dhabi, United Arab Emirates

    • Sandra Goutte
  6. Department of Integrative Biology, University of Texas, Austin, TX, USA

    • Michael J. Ryan

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Contributions

W.H. and J.E. conceived the study and designed the experiments. M.B., L.K., N.H. and S.G. collected the field data. M.B., L.K., S.G. and W.H. analysed the data. W.H., J.E., R.A.P., P.A.T., X.E.B. and M.J.R. discussed the results and wrote the paper.

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The authors declare no competing interests.

Corresponding author

Correspondence to Wouter Halfwerk.

Supplementary information

  1. Supplementary Information

    Supplementary Tables 1–3

  2. Reporting Summary

  3. Supplementary Data 1

    Example call of a forest male frog recorded along pipeline road. Sound file belonging to spectrogram of forest male shown in Figure 2

  4. Supplementary Data 2

    Example call of an urban male recorded in the town of Gamboa. Sound file belonging to spectrogram of urban male shown in Figure 2

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DOI

https://doi.org/10.1038/s41559-018-0751-8