Evolutionary Biology

, Volume 40, Issue 1, pp 141–149 | Cite as

Assessing the Patterns of Evolution in Anuran Vocal Sexual Signals

  • Morgan J. McLeanEmail author
  • Phillip J. Bishop
  • Shinichi Nakagawa
Research Article


Many animal species have evolved signalling traits to mediate various intra-specific interactions. Signals are particularly important for inter-sexual selection, where females use male signalling traits to select mates. Female preferences are therefore a major selective force in the evolution of these male signals, and these preferences can facilitate rapid changes in these traits in an evolutionary timeframe. This introduction of high levels of variation in inter-sexual signals may overshadow any phylogenetic patterns present. Such shadowing effects, however, should be dependant on the characteristics of traits (e.g. morphological, physiological and behavioural). Using male advertisement calls from 72 species of anuran amphibians, we tested the levels of phylogenetic signal present for a variety of call features in relation to trait types, and for calls as whole units using phylogenetic principal components analysis. We found that most call features displayed some level of phylogenetic autocorrelation (or signal), with traits that are dependent on morphology having much stronger phylogenetic signals than those based on behaviour. In addition, when calls were analysed as whole units, closely related species were found to be similar to each other, indicating that phylogenetic patterns had not been cancelled out by selection via female preferences. We suggest that signal functions, such as indicating male quality (e.g. mediated by body size) to potential mates, may place constraints on the amount of variation that can be introduced by female preferences. More research, particularly studies on other taxa, will be required to elucidate whether the patterns found in anurans are general across the animal kingdom.


Comparative analysis Phylogenetic analysis Frog Sexual selection 



We would like to thank the Macaulay Library, and the British Library for providing the sound files used in this analysis. We also thank the SN Behavioural Ecology lab members for discussion and comments on the manuscript. Finally, we would like to thank two anonymous reviewers for their useful comments and suggestions. M.J.M. is supported by the University of Otago Postgraduate Award.

Supplementary material

11692_2012_9197_MOESM1_ESM.docx (59 kb)
Supplementary material 1 (DOCX 58 kb)


  1. Abouheif, E. (1999). A method for testing the assumption of phylogenetic independence in comparative data. Evolutionary Ecology Research, 1(8), 895–909.Google Scholar
  2. Akre, K. L., Farris, H. E., Lea, A. M., Page, R. A., & Ryan, M. J. (2011). Signal perception in frogs and bats and the evolution of mating signals. Science, 333(6043), 751–752.PubMedCrossRefGoogle Scholar
  3. Alexander-Pyron, R., & Wiens, J. J. (2011). A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution, 61(2), 543–583.CrossRefGoogle Scholar
  4. Andersson, M., & Simmons, L. W. (2006). Sexual selection and mate choice. Trends in Ecology and Evolution, 21(6), 296–302.PubMedCrossRefGoogle Scholar
  5. Beecher, M. D. (1989). Signaling systems for individual recognition—An information theory approach. Animal Behaviour, 38, 248–261.CrossRefGoogle Scholar
  6. Berven, K. A. (1981). Mate choice in the wood frog, Rana sylvatica. Evolution, 35(4), 707–722.CrossRefGoogle Scholar
  7. Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioural traits are more labile. Evolution, 57(4), 717–745.PubMedGoogle Scholar
  8. Bosch, J., & De la Riva, I. (2004). Are frog calls modulated by the environment? An analysis with anuran species from Bolivia. Canadian Journal of Zoology, 82(6), 880–888.CrossRefGoogle Scholar
  9. Botero, C. A., Rossman, R. J., Caro, L. M., Stenzler, L. M., Lovette, I. J., de Kort, S. R., et al. (2009). Syllable type consistency is related to age, social status and reproductive success in the tropical mockingbird. Animal Behaviour, 77(3), 701–706.PubMedCrossRefGoogle Scholar
  10. Brown, J., Morales, V., & Summers, K. (2010). A key ecological trait drove the evolution of biparental care and monogamy in an amphibian. American Naturalist, 175, 436–446.PubMedCrossRefGoogle Scholar
  11. Byers, B. E. (2007). Extrapair paternity in chestnut-sided warblers is correlated with consistent vocal performance. Behavioral Ecology, 18(1), 130–136.CrossRefGoogle Scholar
  12. Capranica, R. R. (1965). The evoked vocal response of the bullfrog: A study of communication by sound. Cambridge: MIT.Google Scholar
  13. Castellano, S., & Giacoma, C. (1998). Stabilizing and directional female choice for male calls in the European green toad. Animal Behaviour, 56, 275–287.PubMedCrossRefGoogle Scholar
  14. Cherry, M. I. (1992). Sexual selection in the leopard toad, Bufo pardalis. Behaviour, 120, 164–176.CrossRefGoogle Scholar
  15. Cocroft, R. B., & Ryan, M. J. (1995). Patterns of advertisement call evolution in toads and chorus frogs. Animal Behaviour, 49(2), 283–303.CrossRefGoogle Scholar
  16. Dieckmann, U., & Doebeli, M. (1999). On the origin of species by sympatric speciation. Nature, 400(6742), 354–357.PubMedCrossRefGoogle Scholar
  17. Dobzhansky, T. (1937). Genetics and the origin of species. New York: Columbia University Press.Google Scholar
  18. Dyson, M. L., Passmore, N. I., Bishop, P. J., & Henzi, S. P. (1992). Male-behavior and correlates of mating success in a natural-population of African painted reed frogs (Hyperolius marmoratus). Herpetologica, 48(2), 236–246.Google Scholar
  19. Fuzessery, Z. M. (1988). Frequency tuning in the anuran central auditory system. In B. Fritzsch, M. J. Ryan, W. Wilczynski, T. Hetherington, & W. Walkowiak (Eds.), The evolution of the amphibian auditory system (pp. 253–273). New York: Wiley.Google Scholar
  20. Gavrilets, S., & Waxman, D. (2002). Sympatric speciation by sexual conflict. Proceedings of the National Academy of Sciences, 99(16), 10533–10538.CrossRefGoogle Scholar
  21. Gerhardt, H. C. (1994). The evolution of vocalization in frogs and toads. Annual Review of Ecology and Systematics, 25, 293–324.CrossRefGoogle Scholar
  22. Gray, D. A., & Cade, W. H. (2000). Sexual selection and speciation in field crickets. Proceedings of the National Academy of Sciences USA, 97(26), 14449–14454.CrossRefGoogle Scholar
  23. Hadfield, J. D. (2010). MCMC methods for multi-response generalized linear mixed models: The MCMCglmm R package. Journal of Statistical Software, 33(2), 1–22.Google Scholar
  24. Hadfield, J. D., & Nakagawa, S. (2010). General quantitative genetic methods for comparative biology: Phylogenies, taxonomies and multi-trait models for continuous and categorical characters. Journal of Evolutionary Biology, 23(3), 494–508.PubMedCrossRefGoogle Scholar
  25. Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003). Measuring inconsistency in meta-analyses. BMJ, 327(7414), 557–560.PubMedCrossRefGoogle Scholar
  26. Jombart, T., Balloux, F., & Dray, S. (2010). Adephylo: New tools for investigating the phylogenetic signal in biological traits. Bioinformatics, 26(15), 1907–1909.PubMedCrossRefGoogle Scholar
  27. Kondrashov, A. S., & Kondrashov, F. A. (1999). Interactions among quantitative traits in the course of sympatric speciation. Nature, 400(6742), 351–354.PubMedCrossRefGoogle Scholar
  28. Krasnov, B. R., Poulin, R., & Mouillot, D. (2011). Scale-dependence of phylogenetic signal in ecological traits of ectoparasites. Ecography, 34(1), 114–122.CrossRefGoogle Scholar
  29. Lesbarreres, D., Merila, J., & Lode, T. (2008). Male breeding success is predicted by call frequency in a territorial species, the agile frog (Rana dalmatina). Canadian Journal of Zoology, 86(11), 1273–1279.CrossRefGoogle Scholar
  30. Lopez, P. T., & Narins, P. M. (1991). Mate choice in the neotropical frog, Eleutherodactylus coqui. Animal Behaviour, 41, 757–772.CrossRefGoogle Scholar
  31. Lynch, M. (1991). Methods for the analysis of comparative data in evolutionary biology. Evolution, 45(5), 1065–1080.CrossRefGoogle Scholar
  32. Marquez, R., & Bosch, J. (1997). Male advertisement call and female preference in sympatric and allopatric midwife toads. Animal Behaviour, 54, 1333–1345.PubMedCrossRefGoogle Scholar
  33. Martin, W. F. (1972). Muscular control of vocal tract during release signaling in toad Bufo valliceps. Journal of Morphology, 137(1), 1–27.PubMedCrossRefGoogle Scholar
  34. Mayr, E. (1982). The growth of biological thought. Diversity, evolution, and inheritance. Cambridge: Harvard University Press.Google Scholar
  35. McLean, M. J., Bishop, P. J., & Nakagawa, S. (2012). Male quality, signal reliability and female choice: Assessing the expectations of inter-sexual selection. Journal of Evolutionary Biology,. doi: 10.1111/j.1420-9101.2012.02533.x.PubMedGoogle Scholar
  36. Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401(6756), 877–884.PubMedCrossRefGoogle Scholar
  37. Passmore, N. I., Capranica, R. R., Telford, S. R., & Bishop, P. J. (1984). Phonotaxis in the painted reed frog (Hyperolius marmoratus). Journal of Comparative Physiology A, 154(2), 189–197.CrossRefGoogle Scholar
  38. Platz, J. E., & Lathrop, A. (1993). Body size and age assessment among advertising male chorus frogs. Journal of Herpetology, 27(1), 109–111.CrossRefGoogle Scholar
  39. R Development Core Team. (2010). R: A language and environment for statistical computing. Vienna, Austria: R Foundation For Statistical Computing.Google Scholar
  40. Ryan, M. J. (1980). Female mate choice in a neotropical frog. Science, 209(4455), 523–525.PubMedCrossRefGoogle Scholar
  41. Ryan, M. J. (1986). Factors influencing the evolution of acoustic communication—Biological constraints. Brain Behaviour and Evolution, 28(1–3), 70–82.CrossRefGoogle Scholar
  42. Ryan, M. J. (1988). Constraints and patterns in the evolution of anuran acoustic communication. In B. Fritzsch (Ed.), The evolution of the amphibian auditory system (pp. 637–677). New York: Wiley.Google Scholar
  43. Scheuber, H., Jacot, A., & Brinkhof, M. W. G. (2003). Condition dependence of a multicomponent sexual signal in the field cricket Gryllus campestris. Animal Behaviour, 65(4), 721–727.CrossRefGoogle Scholar
  44. Schwartz, J. J. (2001). Call monitoring and interactive playback systems in the study of acoustic interactions among male anurans. In M. J. Ryan (Ed.), Anuran communication (pp. 183–204). Washington, DC: Smithsonian Institution Press.Google Scholar
  45. Searcy, W. A., & Nowicki, S. (2005). The evolution of animal communication: Reliability and deception in signaling systems. Princeton, New Jersey: Princeton University Press.Google Scholar
  46. Smith, J. M., & Harper, D. (2003). Animal signals. Oxford: Oxford University Press.Google Scholar
  47. van Doorn, G. S., Edelaar, P., & Weissing, F. J. (2009). On the origin of species by natural and sexual selection. Science, 326(5960), 1704–1707.PubMedCrossRefGoogle Scholar
  48. Wagner, W. E. (1989). Graded aggressive signals in Blanchard cricket frog—Vocal responses to opponent proximity and size. Animal Behaviour, 38, 1025–1038.CrossRefGoogle Scholar
  49. Wells, K. D. (1977a). The social behaviour of anuran amphibians. Animal Behaviour, 25, 666–693.CrossRefGoogle Scholar
  50. Wells, K. D. (1977b). Territoriality and male mating success in the green frog (Rana clamitans). Ecology, 58(4), 750–762.CrossRefGoogle Scholar
  51. Winquist, T., & Lemon, R. E. (1994). Sexual selection and exaggerated male tail length in birds. The American Naturalist, 143(1), 95–116.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Morgan J. McLean
    • 1
    Email author
  • Phillip J. Bishop
    • 1
  • Shinichi Nakagawa
    • 1
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand

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