Login to MyKarger

New to MyKarger? Click here to sign up.



Login with Facebook

Forgot your password?

Authors, Editors, Reviewers

For Manuscript Submission, Check or Review Login please go to Submission Websites List.

Submission Websites List

Institutional Login
(Shibboleth or OpenAthens)

For the academic login, please select your country in the dropdown list. You will be redirected to verify your credentials.

Original Paper

Evolution of Calls and Auditory Tuning in the Physalaemus pustulosus Species Group

Wilczynski W.a · Rand A.S.b · Ryan M.J.b,c

Author affiliations

Department of aPsychology and Institute for Neuroscience, University of Texas at Austin, bSmithsonian Tropical Research Institute, Balboa, Republic of Panama, and cSection of Integrative Biology, University of Texas, Austin, Tex., USA

Related Articles for ""

Brain Behav Evol 2001;58:137–151

Do you have an account?

Login Information





Contact Information











I have read the Karger Terms and Conditions and agree.



Login Information





Contact Information











I have read the Karger Terms and Conditions and agree.



To view the fulltext, please log in

To view the pdf, please log in

Buy

  • FullText & PDF
  • Unlimited re-access via MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

CHF 9.00 *
EUR 8.00 *
USD 9.00 *

Select

KAB

Buy a Karger Article Bundle (KAB) and profit from a discount!

If you would like to redeem your KAB credit, please log in.


Save over 20% compared to the individual article price.
Learn more

Rent/Cloud

  • Rent for 48h to view
  • Buy Cloud Access for unlimited viewing via different devices
  • Synchronizing in the ReadCube Cloud
  • Printing and saving restrictions apply

Rental: USD 8.50
Cloud: USD 20.00


Select

Subscribe

  • Access to all articles of the subscribed year(s) guaranteed for 5 years
  • Unlimited re-access via Subscriber Login or MyKarger
  • Unrestricted printing, no saving restrictions for personal use
read more

Subcription rates


Select

* The final prices may differ from the prices shown due to specifics of VAT rules.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Published online: March 07, 2002
Issue release date: 2001

Number of Print Pages: 15
Number of Figures: 6
Number of Tables: 2

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE

Abstract

In species within the Physalaemus pustulosus species group, male frogs produce a whine-like advertisement call consisting of a frequency sweep typically descending from 1,000 to 400 Hz (depending on the species). One species, Physalaemus pustulosus, the túngara frog, has evolved a second call syllable, the chuck, which males place after their whine. Most energy in the chuck is above 1,500 Hz and peaks at 2,400 Hz. We investigated whether the evolution of this new call component in P. pustulosus coincided with evolution of auditory tuning. We used multiunit electrophysiological recordings of auditory-evoked activity in the midbrain to characterize auditory tuning in Physalaemus pustulosus, four other Physalaemus species within the P. pustulosus clade, and three additional, closely related Physalaemus species as outgroups. All eight species had similar sensitivity profiles, with a broad area of enhanced sensitivity from 100 to 1,100 Hz, which we presume represents amphibian papilla (AP) tuning, and a second, narrower area of enhanced sensitivity centered above 2,100 Hz, which we presume represents basilar papilla (BP) tuning. For all species, the whine stimulates the AP. The P. pustulosus chuck stimulates the BP. The frequency with greatest AP sensitivity differed significantly among species. Although in all cases the AP peak lay within the frequency sweep of the whine, phylogenetically corrected correlations revealed no significant relationships between AP tuning and any spectral feature of the whine. BP tuning was similar among all species, with mean BP best excitatory frequencies (BEFs) around 2,100–2,200 Hz, with the exception of P. pustulatus, with a mean BP BEF of 2,549 Hz. Physalaemus pustulosus, the only investigated species that produces a call component stimulating the BP, had a BP BEF that was not significantly different from any of the species within its clade except P. pustulatus, or from any of the outgroup species. A phylogenetic reconstruction of ancestral BP tuning confirms that the only point of evolutionary change in BP tuning is in the line of descent leading to P. pustulatus, not in the line leading to P. pustulosus despite this being the species using the BP for communication. The results indicate that BP tuning around 2,200 Hz is a conserved trait in the Physalaemus pustulosus species group and that no evolution of BP tuning accompanied the subsequent evolution of the call component (the chuck) that stimulates it. This supports the sensory exploitation idea, which posits that signals evolve to match preexisting features of receiver systems.

© 2002 S. Karger AG, Basel


References

  1. Alexander, R.D. (1962) Evolutionary change in cricket acoustical communication. Evolution, 16: 443–467.
  2. Beeman, K. (1996) Signal. Engineering Design, Belmont, MA.
  3. Boake, C.R.B. (1991) Coevolution of senders and receivers of sexual signals: Genetic coupling and genetic correlations. Trends Ecol. Evol., 6: 225–231.
  4. Borgia, G., and S.W. Coleman (2000) Co-option of male courtship signals from aggressive display in bowerbirds. Proc. R. Soc. Biol. Sci. B, 267: 1735–1740.
  5. Bradbury, J.W., and S.L. Vehrencamp (1998) Principles of Animal Communication. Sinauer Assoc. Inc., Sunderland, MA.
  6. Bradbury, J.W., and S.L. Vehrencamp (2000) Economic models of animal communication. Anim. Behav., 59: 259–268.
    External Resources
  7. Brenowitz, E.A., W. Wilczynski, and H.H. Zakon (1984) Acoustic communication in spring peepers: Environmental and behavioral aspects. J. Comp. Physiol. A., 155: 585–592.
  8. Burda, H., V. Bruns, and M. Muller (1990) Sensory adaptations in subterranean mammals. Prog. Clin. Biol. Res., 335: 269–293.
  9. Cannatella, D.C., D.M. Hillis, P. Chippinendale, L. Weigt, A.S. Rand, and M.J. Ryan (1998) Phylogeny of frogs of the Physalaemus pustulosus species group, with an examination of data incongruence. Syst. Biol., 47: 311–335.
  10. Capranica, R.R. (1965) The Evoked Vocal Response of the Bullfrog: A Study of Communication by Sound. MIT Press, Cambridge, MA.
  11. Capranica, R.R. (1966) Vocal response of the bullfrog to natural and synthetic mating calls. J. Acoust. Soc. Am., 40: 1131–1139.
  12. Capranica, R.R. (1968) The vocal repertoire of the bullfrog (Rana catesbeiana). Behaviour, 21:302–325.
  13. Capranica, R.R., and A.J.M. Moffat (1980) Nonlinear properties of the peripheral auditory system of anurans. In Comparative Studies of Hearing in Vertebrates (ed. by A.N. Popper and R.R. Fay), Springer-Verlag, New York, pp. 139–165.
  14. Capranica, R.R., and A.J.M. Moffat (1983) Neurobehavioral correlates of sound communication in anurans. In Advances in Vertebrate Neuroethology (ed. by J.-P. Ewert, R.R. Capranica and D. Ingle), Plenum Press, New York, pp. 701–730.
  15. Carew, T.J. (2000) Behavioral Neurobiology, The Cellular Organization of Behavior. Sinauer Assoc. Inc., Sunderland, MA.
  16. Doherty, J., and R.R. Hoy (1985) Communication in insects III. The auditory behavior of crickets: Some views of genetic coupling, song recognition, and predator detection. Quart. Rev. Biol., 60: 453–472.
  17. Endler, J.A. (1992) Signals, signal conditions, and the direction of evolution. Am. Nat., 139: S125–S153.
    External Resources
  18. Endler, J.A., and A.L. Basolo (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol. Evol., 13: 415–420.
  19. Felsenstein, J. (1985) Phylogenies and the comparative method. Am. Nat. 125: 1–15.
  20. Gerhardt, H.C., and J.J. Schwartz (2001) Auditory tuning and frequency preferences in anurans. In Anuran Communication (ed. by M.J. Ryan), Smithsonian Institution Press, Washington D.C., pp 73–85.
  21. Hauser, M.D. (1996) The Evolution of Animal Communication. MIT Press, Cambridge, MA.
  22. Hoy, R.R., J. Hahn, and R.C. Paul (1977) Hybrid cricket auditory behavior: Evidence for genetic coupling in animal communication. Science, 195: 82–84.
    External Resources
  23. Keddy-Hector, A.C., W. Wilczynski, and M.J. Ryan (1992) Call patterns and basilar papilla tuning in cricket frogs. II. Intrapopulational variation and allometry. Brain Behav. Evol., 39: 238–246.
  24. Lewis, E.R. (1984) On the frog amphibian papilla. Scan. Electron Microsc., 1984: 1899–1913.
  25. Lewis, E.R. (1987) Speculations about noise and the evolution of vertebrate hearing. Hear. Res., 25: 83–90.
  26. Lewis, E.R., and R.E. Lombard (1988) The amphibian inner ear. In The Evolution of the Amphibian Auditory System (ed. by B. Fritzsch, M.J. Ryan, W. Wilczynski, T.E. Hetherington and W. Walkowiak), Wiley, New York, pp. 93–123.
  27. Lewis, E.R., and P.M. Narins (1999) The acoustic periphery of amphibians: Anatomy and physiology. In Comparative Hearing: Fish and Amphibians (ed. by R.R. Fay and A.N. Popper), Springer-Verlag, New York, pp. 101–154.
  28. Lewis, E.R., E.I. Hecht and P.M. Narins (1992) Diversity of form in the amphibian papilla of Puerto Rican frogs. J. Comp. Physiol. A, 171: 421–435.
    External Resources
  29. Loftus-Hills, J.J. (1973) Comparative aspects of auditory function in Australian anurans. Aust. J. Zool., 21: 353–367.
  30. Martins, E.P. (2001) COMPARE, version 4.4. Computer programs for the statistical analysis of comparative data. Distributed by the author via the www at http://compare.bio.indiana. edu/. Department of Biology, Indiana University, Bloomington, IN.
  31. Martins, E.P., and T.F. Hansen (1997) Phylogenies and the comparative method: A general approach to incorporating phylogenetic information into analysis of interspecific data. Am. Nat., 149: 646–667.
  32. McClelland, B.E., W. Wilczynski, and A.S. Rand (1997) Sexual dimorphism and species differences in the neurophysiology and morphology of the acoustic communication system of two neotropical hylids. J. Comp. Physiol. A., 180: 451–462.
  33. McClelland, B.E., W. Wilczynski, and M.J. Ryan (1996) Correlations between call characteristics and morphology in male cricket frogs (Acris crepitans). J. Exp Biol., 199: 1907–1919.
    External Resources
  34. Narins, P.M., and R.R. Capranica (1976) Sexual differences in the auditory system of the tree frog Eleutherodactylus coqui. Science, 192: 378–380.
    External Resources
  35. Oelschläger, H.H.A., M. Nakamura, M. Herzog, and H. Burda (2000) Visual system labeled by c-Fos immunohistochemistry after light exposure in the ‘blind’ subterranean Zambian mole rat (Cryptomys anselli). Brain Behav. Evol., 55: 209–220.
  36. Phelps, S.M., A.S. Rand, and M.J. Ryan (in review) Túngara frogs eavesdrop on heterospecific calls: The predation-rumor hypothesis and the function of a sensory bias. Anim. Behav.
  37. Purgue, A.P., and P.M. Narins (2000) Mechanics of the inner ear of the bullfrog (Rana catesbeiana): the contact membranes and the periotic canal. J. Comp. Physiol. A., 186: 481–488.
  38. Ryan, M.J. (1980) Female mate choice in a neotropical frog. Science, 209: 523–525.
  39. Ryan, M.J. (1985) The Túngara Frog. A Study in Sexual Selection. University of Chicago Press, Chicago, IL.
  40. Ryan, M.J. (1986) Neuroanatomy influences speciation rate in anurans. Proc. Nat. Acad. Sci., 83: 1379–1382.
  41. Ryan, M.J. (1990) Sexual selection, sensory systems, and sensory exploitation. Oxford Surv. Evol. Biol., 7: 46–52.
  42. Ryan, M.J. (1997) Sexual selection and mate choice. In Behavioral Ecology, an Evolutionary Approach, Fourth Edition (ed. by J.R. Krebs and N.R. Davis), Blackwell, Oxford, pp. 179–202.
  43. Ryan, M.J. (1998) Receiver biases, sexual selection and the evolution of sex differences. Science, 281: 1999–2003.
  44. Ryan, M.J., and A.S. Rand (1993) Phylogenetic patterns of behavioral mate recognition systems in Physalaemus pustulosus species (Anura: Leptodactyllidae): the role of ancestral and derived characters and sensory exploitation. Linnean Soc. Symp. Ser., 14: 251–267.
  45. Ryan, M.J., and A.S. Rand (1995) Female responses to ancestral advertisement calls in the túngara frog. Science, 269: 390–392.
  46. Ryan, M.J., and A.S. Rand (1998) Evoked vocal response in male túngara frogs: Preexisting biases in male responses? Anim. Behav., 56:1509–1516.
  47. Ryan, M.J., and A.S. Rand (1999) Phylogenetic inference and the evolution of communication in túngara frogs. In The Design of Animal Communication (ed. by M. Hauser and M. Konishi), MIT Press, Cambridge, Mass., pp. 535–557.
  48. Ryan, M.J., and A.S. Rand (2001) Feature weighting in signal recognition and discrimination by túngara frogs. In Anuran Communication (ed. by M.J. Ryan), Smithsonian Institution Press, Washington D.C., pp. 86–101.
  49. Ryan, M.J., and W. Wilczynski (1988) Coevolution of sender and receiver: Effect on local mate preferences in cricket frogs. Science, 240: 1786–1788.
  50. Ryan, M.J., and W. Wilczynski (1991) Evolution of intraspecific variation in the advertisement call of a cricket frog (Acris crepitans, Hylidae). Biol. J. Linn. Soc., 44: 249–271.
  51. Ryan, M.J., J.H. Fox, W. Wilczynski, and A.S. Rand (1990) Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature, 343: 66–67.
  52. Ryan, M.J., S.A. Perrill, and W. Wilczynski (1992) Auditory tuning and call frequency predict population-based mating preferences in the cricket frog, Acris crepitans. Am. Nat., 139:1370–1383.
  53. Shaw, K. (1995) Phylogenetic tests of the sensory exploitation model of sexual selection. Trends Ecol. Evol., 10: 117–120.
  54. Shofner, W.P., and A.S. Feng (1981) Post-metamorphic development of frequency selectivities and sensitivities of the peripheral auditory system of the bullfrog, Rana catesbeiana. J. Exp. Biol., 93: 181–196.
  55. Smotherman, M.S., and P.M. Narins (1999) The electrical properties of auditory hair cells in the frog amphibian papilla. J. Neurosci., 19: 5275–5292.
    External Resources
  56. Smotherman, M.S., and P.M. Narins (2000) Hair cells, hearing and hopping: A field guide to hair cell physiology in the frog. J. Exp. Biol., 203:2237–2246.
  57. Tárano, Z., and M.J. Ryan (in review) No preexisting biases for heterospecific call traits in the frog Physalaemus enesefae. Anim. Behav.
  58. Tuttle, M.D., L.K. Taft, and M.J. Ryan (1982) Evasive behaviour of a frog in response to bat predation. Anim. Behav., 30: 393–397.
  59. Voneida, T.J., and S.E. Fish (1984) Central nervous system changes related to the reduction of visual input in a naturally blind fish (Astyanax hubbsi). Am. Zool., 24: 775–782.
  60. Wever, E.G. (1985) The Amphibian Ear. Princeton University Press, Princeton, NJ.
  61. Wilczynski, W. (1986) Sexual differences in neural tuning and their effect on active space. Brain Behav. Evol., 28: 83–94.
    External Resources
  62. Wilczynski, W., and R.R. Capranica (1984) The auditory system of anuran amphibians. Prog. Neurobiol., 22: 1–38.
  63. Wilczynski, W., A.C. Keddy-Hector, and M.J. Ryan (1992) Call patterns and basilar papilla tuning in cricket frogs. I. Differences among populations and between sexes. Brain Behav. Evol., 39: 229–237.
  64. Wilczynski, W., B.E. McClelland, and A.S. Rand (1993) Acoustic, auditory, and morphological divergence in three species of neotropical frog. J. Comp. Physiol. A., 172: 425–438.
    External Resources
  65. Wilczynski, W., A.S. Rand, and M.J. Ryan (1995) The processing of spectral cues by the call analysis system of the túngara frog, Physalaemus pustulosus. Anim. Behav., 49: 911–929.
    External Resources
  66. Wilczynski, W., A.S. Rand, and M.J. Ryan (1999) Female preferences for temporal order of call components in the túngara frog: a Bayesian analysis. Anim. Behav., 58: 841–851.
  67. Wilczynski, W., H.H. Zakon, and E.A. Brenowitz (1984) Acoustic communication in spring peepers. Call characteristics and neurophysiological aspects. J. Comp. Physiol. A., 155: 577–584.
  68. Wilkens, H. (1971) Genetic interpretation of regressive evolutionary processes: studies on hybrid eyes of two Astyanax populations (Characidae, Pices). Evolution, 25: 530–544.
  69. Wilkinson, L. (1996) Systat. SPSS Science Marketing Dept, Chicago, Ill.
  70. Zakon, H.H., and W. Wilczynski (1988) The physiology of the anuran eighth nerve. In The Evolution of the Amphibian Auditory System (ed. by B. Fritzsch, M.J. Ryan, W. Wilczynski, T.E. Hetherington and W. Walkowiak), Wiley, New York, pp. 125–155.

Article / Publication Details

First-Page Preview
Abstract of Original Paper

Published online: March 07, 2002
Issue release date: 2001

Number of Print Pages: 15
Number of Figures: 6
Number of Tables: 2

ISSN: 0006-8977 (Print)
eISSN: 1421-9743 (Online)

For additional information: https://www.karger.com/BBE


Copyright / Drug Dosage / Disclaimer

Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.