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Post-mating clutch piracy in an amphibian

Abstract

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.

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Acknowledgements

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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Supplementary Material

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). https://doi.org/10.1038/nature02879

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