Behavioral Ecology and Sociobiology

, Volume 59, Issue 6, pp 796–804 | Cite as

No evidence for female mate choice based on genetic similarity in the túngara frog Physalaemus pustulosus

  • Kathrin P. Lampert
  • Ximena E. Bernal
  • A. Stanley Rand
  • Ulrich G. Mueller
  • Michael J. Ryan
Original Article


In most sexually reproducing animals, the behavior of one or both sexes during courtship critically influences the success at mating of the opposite sex. This behavior is often interpreted as “mate choice,” and there is great interest in why such choices are exercised. The explanation for the evolution of mate choice that has received the most attention and generated the most controversy is based on assumed genetic effects. In this study, we investigated whether female túngara frogs, which choose mates based on acoustic cues, have a preference for genetically less related males. Specifically, we determine if there is disassortive mating based on microsatellite markers, if there is information in the advertisement call that could be used to assess genetic similarity, and if females exhibit acoustic-based mating preferences that would promote choice for genetic diversity. Using seven microsatellite markers, we found no correlation of male call similarity and male genetic relatedness. Female choice experiments showed no female preference for calls of less related males, and there was no evidence for inbreeding avoidance in the field. Our results do not support the hypothesis of mate choice based on information about genetic relatedness conveyed by acoustic signals in túngara frogs.


Animal communication Mate choice Relatedness Microsatellite marker Sexual selection 



We wish to thank Autoridad National del Ambiente of the Republic of Panama and the Smithsonian Tropical Research Institute (STRI) for research and export permits. STRI provided invaluable logistic support. We are especially indebted to H. Pröhl, who developed the microsatellite primers used in this study. The critical comments of T. Juenger and B. Waldman greatly improved the manuscript. This work was supported by the German Science Foundation (DFG) LA 1382/2-1 (KPL), by National Science Foundation (NSF) grants IBN-0078184 to M.J.R., D. Cannatella, and W. Wilczynski, and IBN-9816564 to M.J.R., and by an NSF-CAREER award DEB-9983879 to U.G.M. The research presented complies with the current laws of the countries in which it was performed.


  1. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  2. Bernatchez L, Landry C (2003) MHC studies in nonmodel vertebrates: What have we learned about natural selection in 15 years? J Evol Biol 16:363–377PubMedCrossRefGoogle Scholar
  3. Blouin MS, Parsons M, Lacaille V, Lotz S (1995) Use of microsatellite loci to classify individuals by relatedness. Mol Ecol 5:393–401CrossRefGoogle Scholar
  4. Coyne JA, Orr HA (1998) The evolutionary genetics of speciation. Philos Trans R Soc Lond B Biol Sci 353:287–305PubMedCrossRefGoogle Scholar
  5. Dobzhansky T (1975) Analysis of incipient reproductive isolation within a species of Drosophila. Proc Natl Acad Sci U S A 72:3638–3641PubMedCrossRefGoogle Scholar
  6. Endler JA (1992) Signals, signal conditions and the direction of evolution. Am Nat 139:S125–S153CrossRefGoogle Scholar
  7. Endler JA, Basolo AL (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol 13:415–420CrossRefGoogle Scholar
  8. Fisher RA (1930) The genetical theory of natural selection. Clarendon, OxfordGoogle Scholar
  9. Gerhardt HC (1994) Reproductive character displacement of female mate choice in the grey treefrog, Hyla chrysoscelis. Anim Behav 47:959–969CrossRefGoogle Scholar
  10. Goodnight KF, Queller DC (1995) Relatedness, version 5.0.8.
  11. Goodnight KF, Queller DC (1996) Kinship 1.3.1.
  12. Grafen A (1990) Sexual selection unhandicapped by the Fisher process. J Theor Biol 144:473–516PubMedGoogle Scholar
  13. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds a role for parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  14. Hankison SJ, Morris MR (2003) Avoiding a compromise between sexual selection and species recognition: female swordtail fish assess multiple species-specific cues. Behav Ecol 14:282–287CrossRefGoogle Scholar
  15. Kirkpatrick M (1982) Sexual selection and the evolution of female choice. Evolution 36:1–12CrossRefGoogle Scholar
  16. Kirkpatrick M, Barton NH (1997) The strength of indirect selection on female mating preferences. Proc Natl Acad Sci U S A 94:1282–1286PubMedCrossRefGoogle Scholar
  17. Kirkpatrick M, Ryan MJ (1991) The paradox of the lek and the evolution of mating preferences. Nature 350:33–38CrossRefGoogle Scholar
  18. Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution of mate choice and mating biases. Proc Biol Sci 270:653–664PubMedCrossRefGoogle Scholar
  19. Lampert KP, Rand AS, Mueller UG, Ryan MJ (2003) Fine-scale genetic pattern and evidence for sex-biased dispersal in the túngara frog, Physalaemus pustulosus. Mol Ecol 12:3325–3334PubMedCrossRefGoogle Scholar
  20. Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci U S A 78:3721–3725PubMedCrossRefGoogle Scholar
  21. Landry C, Garant D, Duchesne P, Bernatchez L (2001) Good genes as heterozygosity: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc Biol Sci 268:1279–1285PubMedCrossRefGoogle Scholar
  22. Lenington S, Coopersmith CB, Erhart M (1994) Female preference and variability among t-haplotypes in wild house mice. Am Nat 143:766–784CrossRefGoogle Scholar
  23. Liedloff A (1999) Mantel version 2.0, Mantel nonparametric test calculator.
  24. Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 157:1753–1766Google Scholar
  25. Marsh D, Rand AS, Ryan MJ (2000) Effects of inter-pond distance on the inbreeding ecology of túngara frogs. Oecologia 122:505–513CrossRefGoogle Scholar
  26. Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, OxfordGoogle Scholar
  27. Mays HL Jr, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554–559PubMedCrossRefGoogle Scholar
  28. Milinski M (2003) The function of mate choice in sticklebacks: optimizing MHC genetics. J Fish Biol 63(Suppl A):1–16CrossRefGoogle Scholar
  29. Mousseau TA, Ritland K, Heath DD (1998) A novel method for estimating heritability using molecular markers. Heredity 80:218–224CrossRefGoogle Scholar
  30. Penn DJ (2002) The scent of genetic compatibility: sexual selection and the major histocompatibility complex. Ethology 108:1–21CrossRefGoogle Scholar
  31. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibiliy complex genes. Am Nat 153:145–169CrossRefGoogle Scholar
  32. Petrie M (1994) Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:598–599CrossRefGoogle Scholar
  33. Pfennig KS (1998) The evolution of mate choice and the potential for conflict between species and mate-quality recognition. Proc R Soc Lond B Biol Sci 265:1742–1748CrossRefGoogle Scholar
  34. Pomiankowski AN (1988) The evolution of female mate preferences for male genetic quality. Oxf Surv Evol Biol 5:136–184Google Scholar
  35. Pröhl H, Adams RMM, Mueller UG, Rand AS, Ryan MJ (2002) Polymerase chain reaction primers for polymorphic microsatellite loci from the túngara frog Physalaemus pustulosus. Mol Ecol Notes 2:341–343CrossRefGoogle Scholar
  36. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  37. Raberg L, Stjernman M, Hasselquist D (2003) Immune responsiveness in adult blue tits: heritability and effects of nutritional status during ontogeny. Oecologia 136:360–364PubMedCrossRefGoogle Scholar
  38. Ritland K, Ritland C (1996) Inferences about quantitative inheritance based on natural population structure in the yellow monkeyflower, Mimulus guttanus. Evolution 50:1074–1082CrossRefGoogle Scholar
  39. Ryan MJ (1980) Female mate choice in a neotropical frog. Science 209:523–525PubMedCrossRefGoogle Scholar
  40. Ryan MJ (1983) Sexual selection and communication in a neotropical frog, Physalaemus pustulosus. Evolution 39:261–272CrossRefGoogle Scholar
  41. Ryan MJ (1985) The túngara frog: a study in sexual selection and communication. University of Chicago Press, ChicagoGoogle Scholar
  42. Ryan MJ (1990) Sensory systems, sexual selection, and sensory exploitation. Oxf Surv Evol Biol 7:157–195Google Scholar
  43. Ryan MJ (1997) Sexual selection and mate choice. In: Krebs JR, Davies NB (eds) Sexual selection and mate choice. Blackwell, Oxford, pp 179–202Google Scholar
  44. Ryan MJ (1998) Receiver biases, sexual selection and the evolution of sex differences. Science 281:1999–2003PubMedCrossRefGoogle Scholar
  45. Ryan MJ, Rand AS (2003) Sexual selection in female perceptual space: how female túngara frogs perceive and respond to complex populations variation in acoustic mating signals. Evolution 57:2608–2618PubMedGoogle Scholar
  46. Shaw K (1995) Phylogenetic tests of the sensory exploitation model of sexual selection. Trends Ecol Evol 10:117–120CrossRefGoogle Scholar
  47. Waldman B, Adler K (1979) Toad tadpoles associate preferentially with siblings. Nature 282:611–613CrossRefGoogle Scholar
  48. Waldman B, Tocher M (1998) Behavioral ecology, genetic diversity, and declining amphibian populations. In: Caro T (ed) Behavioral ecology and conservation biology. Oxford University Press, New York, pp 394–443Google Scholar
  49. Waldman B, Bishop PJ (2004) Chemical communication in an archaic anuran amphibian. Behav Ecol 15:88–93CrossRefGoogle Scholar
  50. Waldman B, Rice JE, Honeycutt RL (1992) Kin recognition and incest avoidance in toads. Am Zool 32:18–30Google Scholar
  51. Wedekind C, Furi S (1997) Body odour preferences in men and women: do they aim for specific MHC combinations or simply heterozygosity? Proc Biol Sci 264:1471–1479PubMedCrossRefGoogle Scholar
  52. Wedekind C, Seebeck T, Bettens F, Paepke AJ (1995) MHC-dependent mate preferences in humans. Proc Biol Sci 260:245–249PubMedCrossRefGoogle Scholar
  53. Welch AM, Semlitsch RD, Gerhardt HC (1998) Call duration as an indicator of genetic quality in male gray tree frogs. Science 280:1928–1930PubMedCrossRefGoogle Scholar
  54. Wells KD (1977) The social behavior of anuran amphibians. Anim Behav 25:666–693CrossRefGoogle Scholar
  55. Yamazaki K, Boyse EA, Mike V, Thaler HT, Mathieson BJ, Abbott J, Boyse J, Zayas ZA, Thomas L (1976) Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med 144:1324–1335PubMedCrossRefGoogle Scholar
  56. Yamazaki K, Beauchamp GK, Shen F, Bard J, Boyse JA (1991) A distinctive change in odor type determined by H-2D/L mutation. Immunogenetics 34:120–131CrossRefGoogle Scholar
  57. Zahavi A (1975) Mate selection: a selection for a handicap. J Theor Biol 53 205–214PubMedCrossRefGoogle Scholar
  58. Zahavi A, Zahavi A (1997) The handicap principle: a missing piece of Darwin’s puzzle. Oxford University Press, OxfordGoogle Scholar
  59. Zelano B, Edwards SV (2002) An MHC component to kin recognition and mate choice in birds: predictions, progress, and prospects. Am Nat 160:S225–S237CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Kathrin P. Lampert
    • 1
  • Ximena E. Bernal
    • 1
  • A. Stanley Rand
    • 2
  • Ulrich G. Mueller
    • 1
    • 2
  • Michael J. Ryan
    • 1
    • 2
  1. 1.Section of Integrative Biology C0930University of TexasAustinUSA
  2. 2.Smithsonian Tropical Research InstituteBalboaPanama

Personalised recommendations