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Post-mating clutch piracy in an amphibian


Female multiple mating and alternative mating systems can decrease the opportunity for sexual selection1,2,3. Sperm competition is often the outcome of females mating with multiple males and has been observed in many animals1,4,5,6,7, and alternative reproductive systems are widespread among species with external fertilization and parental care3,8,9,10. Multiple paternity without associated complex behaviour related to mating or parental care is also seen in simultaneously spawning amphibians11,12,13,14,15 and fishes16 that release gametes into water. Here we report ‘clutch piracy’ in a montane population of the common frog Rana temporaria, a reproductive behaviour previously unknown in vertebrates with external fertilization. Males of this species clasp the females and the pair deposits one spherical clutch of eggs. No parental care is provided. ‘Pirate’ males search for freshly laid clutches, clasp them as they would do a female and fertilize the eggs that were left unfertilized by the ‘parental’ male. This behaviour does not seem to be size-dependent, and some males mate with a female and perform clutch piracy in the same season. Piracy affected 84% of the clutches and in some cases increased the proportion of eggs fertilized, providing direct fitness benefits both for the pirate males and the females17. Sexual selection—probably caused by a strong male-biased sex ratio—occurs in this population, as indicated by size-assortative mating; however, clutch piracy may reduce its impact. This provides a good model to explore how alternative mating strategies can affect the intensity of sexual selection.

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Figure 1: Schematic representation of mating systems in R. temporaria.
Figure 2: Images of clutch piracy in R. temporaria.
Figure 3: Percentage of fertilized eggs in clutches not exposed (grey) and exposed (black) to clutch piracy.


  1. Shuster, S. M. & Wade, M. J. Mating Systems and Strategies. Monographs in Behavior and Ecology (Princeton Univ. Press, New Jersey, 2003)

    Google Scholar 

  2. Jones, A. G., Walker, D., Kvarnemo, C., Lindstroem, K. & Avise, J. C. How cuckoldry can decrease the opportunity for sexual selection: Data and theory from a genetic parentage analysis of the sand goby, Potamoschistus minutus. Proc. Natl Acad. Sci. USA 98, 9151–9156 (2001)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Avise, J. C. et al. Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. Annu. Rev. Genet. 36, 19–45 (2002)

    CAS  Article  PubMed  Google Scholar 

  4. Birkhead, T. R. & Parker, G. A. in Behavioural Ecology: An Evolutionary Approach (eds Krebs, J. R. & Davies, N. B.) 121–148 (Blackwell, Oxford, 1997)

    Google Scholar 

  5. Olsson, M. & Madsen, T. Promiscuity in sand lizards (Lacerta agilis) and adder snakes (Vipera berus): causes and consequences. J. Hered. 92, 190–197 (2001)

    CAS  Article  PubMed  Google Scholar 

  6. Pearse, D. E. & Avise, J. C. Turtle mating systems: behavior, sperm storage, and genetic paternity. J. Hered. 92, 206–211 (2001)

    CAS  Article  PubMed  Google Scholar 

  7. Garner, T. W. J. & Schmidt, B. R. Relatedness, body size and paternity in the alpine newt, Triturus alpestris. Proc. R. Soc. Lond. B 270, 619–624 (2003)

    Article  Google Scholar 

  8. Neff, B. D. Stabilizing selection on genomic divergence in a wild fish population. Proc. Natl Acad. Sci. USA 101, 2381–2385 (2004)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Taborsky, M. The evolution of bourgeois, parasitic, and cooperative reproductive behaviors in fishes. J. Hered. 92, 100–110 (2001)

    CAS  Article  PubMed  Google Scholar 

  10. Clutton-Brock, T. H. The Evolution of Parental Care. Monographs in Behavior and Ecology (Princeton Univ. Press, New Jersey, 1991)

    Google Scholar 

  11. D'Orgeix, C. A. & Turner, B. J. Multiple paternity in the red-eye treefrog Agalychnis callidryas (Cope). Mol. Ecol. 4, 505–508 (1995)

    CAS  Article  PubMed  Google Scholar 

  12. Laurila, A. & Seppa, P. Multiple paternity in the common frog (Rana temporaria): genetic evidence from tadpole kin groups. Biol. J. Linn. Soc. 63, 221–232 (1998)

    Google Scholar 

  13. Byrne, P. G. & Roberts, J. D. Simultaneous mating with multiple males reduces fertilization success in the myobatrachid frog Crinia georgiana. Proc. R. Soc. Lond. B 266, 717–721 (1999)

    Article  Google Scholar 

  14. Roberts, J. D., Standish, R. J., Byrne, P. G. & Doughty, P. Synchronous polyandry and multiple paternity in the frog Crinia georgiana (Anura: Myobatrachidae). Anim. Behav. 57, 721–726 (1999)

    CAS  Article  PubMed  Google Scholar 

  15. Lodé, T. & Lesbarrères, D. Multiple paternity in Rana dalmatina, a monogamous territorial breeding anuran. Naturwissenschaften 91, 44–47 (2004)

    ADS  Article  PubMed  Google Scholar 

  16. Bekkevold, D., Hansen, M. M. & Loeschcke, V. Male reproductive competition in spawning aggregations of cod (Gadus morhua, L.). Mol. Ecol. 11, 91–102 (2002)

    CAS  Article  PubMed  Google Scholar 

  17. Jennions, M. D. & Petrie, M. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75, 21–64 (2000)

    CAS  Article  PubMed  Google Scholar 

  18. Duellman, W. E. & Trueb, L. Biology of Amphibians 1–696 (The Johns Hopkins Univ. Press, Baltimore and London, 1986)

    Google Scholar 

  19. Grossenbacher, K., et al. in Atlas of Amphibians and Reptiles in Europe (ed. Gasc, J. P.) 158–159 (Societas Europaea Herpetologica and Muséum National d'Histoire Naturelle (IEGB/SPN), Paris, 1997)

    Google Scholar 

  20. Elmberg, J. Long-term survival, length of breeding season, and operational sex ratio in a boreal population of common frogs, Rana temporaria L. Can. J. Zool. 68, 121–127 (1990)

    Article  Google Scholar 

  21. Byrne, P. G., Roberts, J. D. & Simmons, L. W. Sperm competition selects for increased testes mass in Australian frogs. J. Evol. Biol. 15, 347–355 (2001)

    Article  Google Scholar 

  22. Gibbons, M. M. & McCarthy, T. K. The reproductive output of frogs Rana temporaria (L.) with particular reference to body size and age. J. Zool. 209, 579–583 (1986)

    Article  Google Scholar 

  23. Elmberg, J. Factors affecting male yearly mating success in the common frog, Rana temporaria. Behav. Ecol. Sociobiol. 28, 125–131 (1991)

    Article  Google Scholar 

  24. Elmberg, J. Random mating in a boreal population of European common frogs Rana temporaria L. Holarc. Ecol. 10, 193–195 (1987)

    Google Scholar 

  25. Foerster, K., Delhey, K., Johnsen, A., Lifjeld, J. T. & Kempenaers, B. Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425, 714–717 (2003)

    ADS  CAS  Article  PubMed  Google Scholar 

  26. Rico, C., Kuhnlein, U. & Fitzgerald, G. J. Male reproductive tactics in the threespine stickleback - an evaluation by DNA fingerprinting. Mol. Ecol. 1, 79–87 (1992)

    Article  Google Scholar 

  27. Jones, A. G., Östlund-Nilsson, S. & Avise, J. C. A microsatellite assessment of sneaked fertilizations and egg thievery in the fifteenspine stickleback. Evolution 52, 848–858 (1998)

    Article  PubMed  Google Scholar 

  28. Vos, C. C., De Jong, A. G., Goedhart, P. W. & Smulders, M. J. M. Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Rana arvalis). Heredity 86, 598–608 (2001)

    CAS  Article  PubMed  Google Scholar 

  29. Marshall, T. C., Slate, J., Kruuk, L. & Pemberton, J. M. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7, 639–655 (1998)

    CAS  Article  PubMed  Google Scholar 

  30. Neff, B. D. & Pitcher, T. E. Assessing the statistical power of genetic analyses to detect multiple mating in fishes. J. Fish Biol. 61, 739–750 (2002)

    Article  Google Scholar 

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We thank T. J. C. Beebee, E. Hespeler and M. Fuerst for help with microsatellite techniques. The team of the Respomuso Refuge (Ursi, Dolores, David, Juani and Javier Abajo), X. González, J. Palanca and N. Palanca provided help and facilities. The Dirección General del Medio Natural de la Diputación General de Aragón issued research permits for the Circo de Piedrafita area. D.R.V. was supported by grants of the University of Vigo, Xunta de Galicia and Deutscher Akademischer Austauschdienst. Grants of the Deutsche Forschungsgemeinschaft to M.V. and A.M. and of the Instituto de Estudios Altoaragoneses to M.V. supported the laboratory work.

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Correspondence to David R. Vieites.

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All supplementary material is included in this file except the video. (DOC 153 kb)

Supplementary Video

This movie is an example of how several males perform clutch piracy with a freshly laid clutch. The video starts showing two pirate males clasping the clutch while repeatedly ejaculate sperm into the egg mass, while other males fight to get access to the clutch. After 16 seconds, one of the pirates releases the clutch and another one immediately replaces his position. This succession of pirate males ejaculating sperm continued for several minutes. (MP4 5474 kb)

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Vieites, D., Nieto-Román, S., Barluenga, M. et al. Post-mating clutch piracy in an amphibian. Nature 431, 305–308 (2004).

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