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.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Fruit bats adjust their foraging strategies to urban environments to diversify their diet
BMC Biology Open Access 16 June 2021
-
Biologia Futura: adaptive changes in urban populations
Biologia Futura Open Access 02 March 2020
-
Linking effective population size dynamics to phenotypic traits in the common toad (Bufo bufo)
Conservation Genetics Open Access 03 May 2019
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
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



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).
References
Steffen, W. et al. Planetary boundaries: guiding human development on a changing planet. Science 347, 1259855 (2015).
Seddon, N. et al. Biodiversity in the Anthropocene: prospects and policy. Proc. R. Soc. B 283, 20162094 (2016).
McKinney, M. L. Urbanisation as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260 (2006).
Marzluff, J., Bowman, R. & Donnelly, R. Avian Ecology and Conservation in an Urbanizing World (Springer, Berlin, 2001).
Alberti, M. et al. Integrating humans into ecology: opportunities and challenges for studying urban ecosystems. Bioscience 53, 1169–1179 (2003).
Grimm, N. B. et al. Global change and the ecology of cities. Science 319, 756–760 (2008).
Alberti, M. Eco-evolutionary dynamics in an urbanizing planet. Trends Ecol. Evol. 30, 114–126 (2015).
Berg, M. P. et al. Adapt or disperse: understanding species persistence in a changing world. Glob. Change Biol. 16, 587–598 (2010).
Slabbekoorn, H. Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds. Anim. Behav. 85, 1089–1099 (2013).
Slabbekoorn, H. & den Boer-Visser, A. Cities change the songs of birds. Curr. Biol. 16, 2326–2331 (2006).
Ripmeester, E. A. P., Kok, J. S., van Rijssel, J. C. & Slabbekoorn, H. Habitat-related birdsong divergence: a multi-level study on the influence of territory density and ambient noise in European blackbirds. Behav. Ecol. Sociobiol. 64, 409–418 (2010).
Lee, J. G. H., MacGregor‐Fors, I. & Yeh, P. J. Sunrise in the city: disentangling drivers of the avian dawn chorus onset in urban greenspaces. J. Avian Biol. 48, 955–964 (2017).
Dominoni, D. M., Greif, S., Nemeth, E. & Brumm, H. Airport noise predicts song timing of European birds. Ecol. Evol. 6, 6151–6159 (2016).
Yeh, P. J. Rapid evolution of a sexually selected trait following population establishment in a novel habitat. Evolution 58, 166–174 (2004).
Gaston, K. J., Bennie, J., Davies, T. W. & Hopkins, J. The ecological impacts of nighttime light pollution: a mechanistic appraisal. Biol. Rev. Camb. Philos. Soc. 88, 912–927 (2013).
Maan, M. E. & Seehausen, O. Ecology, sexual selection and speciation. Ecol. Lett. 14, 591–602 (2011).
Wilkins, M. R., Seddon, N. & Safran, R. J. Evolutionary divergence in acoustic signals: causes and consequences. Trends Ecol. Evol. 28, 156–166 (2013).
Panhuis, T. M., Butlin, R., Zuk, M. & Tregenza, T. Sexual selection and speciation. Trends Ecol. Evol. 16, 364–371 (2001).
Trillo, P., Athanas, K., Goldhill, D., Hoke, K. & Funk, W. The influence of geographic heterogeneity in predation pressure on sexual signal divergence in an Amazonian frog species complex. J. Evol. Biol. 26, 216–222 (2013).
Warren, P. S., Katti, M., Ermann, M. & Brazel, A. Urban bioacoustics: it’s not just noise. Anim. Behav. 71, 491–502 (2006).
Slabbekoorn, H., Yang, X. J. & Halfwerk, W. Birds and anthropogenic noise: singing higher may matter (a comment on Nemeth and Brumm, “Birds and anthropogenic noise: are urban songs adaptive?”). Am. Nat. 180, 142–145 (2012).
Nemeth, E. & Brumm, H. Birds and anthropogenic noise: are urban songs adaptive? Am. Nat. 176, 465–475 (2010).
Montague, M. J., Danek-Gontard, M. & Kunc, H. P. Phenotypic plasticity affects the response of a sexually selected trait to anthropogenic noise. Behav. Ecol. 24, 343–348 (2013).
Swaddle, J. P. et al. A framework to assess evolutionary responses to anthropogenic light and sound. Trends Ecol. Evol. 30, 550–560 (2015).
Halfwerk, W. & Slabbekoorn, H. Pollution going multimodal: the complex impact of the human-altered sensory environment on animal perception and performance. Biol. Lett. 11, 20141051 (2015).
Morley, E. L., Jones, G. & Radford, A. N. The importance of invertebrates when considering the impacts of anthropogenic noise. Proc. R. Soc. B 281, 20132683 (2014).
Lampe, U., Reinhold, K. & Schmoll, T. How grasshoppers respond to road noise: developmental plasticity and population differentiation in acoustic signalling. Funct. Ecol. 28, 660–668 (2014).
Sun, J. W. C. & Narins, P. A. Anthropogenic sounds differentially affect amphibian call rate. Biol. Conserv. 121, 419–427 (2005).
Luther, D. & Baptista, L. Urban noise and the cultural evolution of bird songs. Proc. R. Soc. B 277, 469–473 (2010).
Gross, K., Pasinelli, G. & Kunc, H. P. Behavioral plasticity allows short-term adjustment to a novel environment. Am. Nat. 176, 456–464 (2010).
Read, J., Jones, G. & Radford, A. N. Fitness costs as well as benefits are important when considering responses to anthropogenic noise. Behav. Ecol. 25, 4–7 (2014).
Halfwerk, W., Bot, S. & Slabbekoorn, H. Male great tit song perch selection in response to noise-dependent female feedback. Funct. Ecol. 26, 1339–1347 (2012).
Halfwerk, W. et al. Low-frequency songs lose their potency in noisy urban conditions. Proc. Natl Acad. Sci. USA 108, 14549–14554 (2011).
Ryan, M. J. The Túngara Frog: A Study in Sexual Selection and Communication (Univ. Chicago Press, Chicago, 1985).
Gridi-Papp, M., Rand, A. S. & Ryan, M. J. Complex call production in the tungara frog. Nature 441, 38 (2006).
Rand, A. S. & Ryan, M. J. The adaptive significance of a complex vocal repertoire in a Neotropical frog. Z. Tierpsychol. 57, 209–214 (1981).
Akre, K. L., Farris, H. E., Lea, A. M., Page, R. A. & Ryan, M. J. Signal perception in frogs and bats and the evolution of mating signals. Science 333, 751–752 (2011).
Bernal, X. E., Rand, A. S. & Ryan, M. J. Acoustic preferences and localization performance of blood-sucking flies (Corethrella coquillett) to túngara frog calls. Behav. Ecol. 17, 709–715 (2006).
Tuttle, M. D. & Ryan, M. J. Bat predation and the evolution of frog vocalizations in the Neotropics. Science 214, 677–678 (1981).
Halfwerk, W., Jones, P., Taylor, R., Ryan, M. J. & Page, R. Risky ripples allow bats and frogs to eavesdrop on a multisensory sexual display. Science 343, 413–416 (2014).
Halfwerk, W., Lea, A. M., Guerra, M., Page, R. A. & Ryan, M. J. Vocal responses to noise reveal the presence of the Lombard effect in a frog. Behav. Ecol. 27, 669–676 (2016).
Rand, A. S., Bridarolli, M. E., Dries, L. & Ryan, M. J. Light levels influence female choice in túngara frogs: predation risk assessment? Copeia 1997, 447–450 (1997).
Gomes, D. G. E. et al. Bats perceptually weight prey cues across sensory systems when hunting in noise. Science 353, 1277–1280 (2016).
McMahon, T. A., Rohr, J. R. & Bernal, X. E. Light and noise pollution interact to disrupt interspecific interactions. Ecology 98, 1290–1299 (2017).
Bernal, X. E., Akre, K. L., Baugh, A. T., Rand, A. S. & Ryan, M. J. Female and male behavioral response to advertisement calls of graded complexity in túngara frogs, Physalaemus pustulosus. Behav. Ecol. Sociobiol. 63, 1269–1279 (2009).
Marler, C. & Ryan, M. Energetic constraints and steroid hormone correlates of male calling behaviour in the túngara frog. J. Zool. 240, 397–409 (1996).
Kime, N. M., Whitney, T. K., Davis, E. S. & Marler, C. A. Arginine vasotocin promotes calling behavior and call changes in male túngara frogs. Brain Behav. Evol. 69, 254–265 (2007).
Atwell, J. W. et al. Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation. Behav. Ecol. 23, 960–969 (2012).
Sol, D., Lapiedra, O. & González-Lagos, C. Behavioural adjustments for a life in the city. Anim. Behav. 85, 1101–1112 (2013).
Møller, A. P. Flight distance of urban birds, predation, and selection for urban life. Behav. Ecol. Sociobiol. 63, 63 (2008).
Halfwerk, W. et al. Environmental conditions limit attractiveness of a complex sexual signal in the túngara frog. Nat. Commun. 8, 1891 (2017).
Dudley, R. & Rand, A. S. Sound production and vocal sac inflation in the túngara frog, Physalaemus pustulosus (Leptodactylidae). Copeia 1991, 460–470 (1991).
Audet, J.-N., Ducatez, S. & Lefebvre, L. The town bird and the country bird: problem solving and immunocompetence vary with urbanization. Behav. Ecol. 27, 637–644 (2016).
Carrete, M. & Tella, J. L. Inter-individual variability in fear of humans and relative brain size of the species are related to contemporary urban invasion in birds. PLoS ONE 6, e18859 (2011).
LaZerte, S. E., Slabbekoorn, H. & Otter, K. A. Learning to cope: vocal adjustment to urban noise is correlated with prior experience in black-capped chickadees. Proc. R. Soc. B 283, 20161058 (2016).
Francis, C. D., Ortega, C. P. & Cruz, A. Noise pollution changes avian communities and species interactions. Curr. Biol. 19, 1415–1419 (2009).
Crooks, K. R. & Soulé, M. E. Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400, 563–566 (1999).
Tan, W. H., Tsai, C. G., Lin, C. & Lin, Y. K. Urban canyon effect: storm drains enhance call characteristics of the Mientien tree frog. J. Zool. 294, 77–84 (2014).
Rand, A. S., Ryan, M. J. & Wilczynski, W. Signal redundancy and receiver permissiveness in acoustic mate recognition by the túngara frog, Physalaemus pustulosus. Am. Zool. 32, 81–90 (1992).
Trillo, P. A. et al. Collateral damage or a shadow of safety? The effects of signalling heterospecific neighbours on the risks of parasitism and predation. Proc. R. Soc. B 283, 20160343 (2016).
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
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
Supplementary Information
Supplementary Tables 1–3
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
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
Rights and permissions
About this article
Cite this article
Halfwerk, W., Blaas, M., Kramer, L. et al. Adaptive changes in sexual signalling in response to urbanization. Nat Ecol Evol 3, 374–380 (2019). https://doi.org/10.1038/s41559-018-0751-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41559-018-0751-8
This article is cited by
-
Increases in intraspecific body size variation are common among North American mammals and birds between 1880 and 2020
Nature Ecology & Evolution (2023)
-
Urban-rural gradients: how landscape changes drive adaptive evolution of plant competitive traits
Evolutionary Ecology (2023)
-
More than noise: light, moon phase, and singing behavior in a passerine
Urban Ecosystems (2022)
-
Fruit bats adjust their foraging strategies to urban environments to diversify their diet
BMC Biology (2021)
-
Biologia Futura: adaptive changes in urban populations
Biologia Futura (2020)