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Sophisticated sperm allocation in male fowl

Abstract

When a female is sexually promiscuous, the ejaculates of different males compete for the fertilization of her eggs1; the more sperm a male inseminates into a female, the more likely he is to fertilize her eggs2. Because sperm production is limited and costly, theory predicts that males will strategically allocate sperm (1) according to female promiscuity1,3,4,5, (2) saving some for copulations with new females3,6,7, and (3) to females producing more and/or better offspring3,8. Whether males allocate sperm in all of these ways is not known, particularly in birds where the collection of natural ejaculates only recently became possible. Here we demonstrate male sperm allocation of unprecedented sophistication in the fowl Gallus gallus. Males show status-dependent sperm investment in females according to the level of female promiscuity; they progressively reduce sperm investment in a particular female but, on encountering a new female, instantaneously increase their sperm investment; and they preferentially allocate sperm to females with large sexual ornaments signalling superior maternal investment. Our results indicate that female promiscuity leads to the evolution of sophisticated male sexual behaviour.

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Figure 1: Differential sperm allocation and female promiscuity.
Figure 2: Preferential sperm investment in new females.
Figure 3: Preferential sperm investment in new females (continued).
Figure 4: Mate choice and strategic sperm allocation by male fowl.

References

  1. Parker, G. A. in Sperm Competition and Sexual Selection (eds Birkhead, T. R. & Møller, A. P.) 3–54 (Academic, London, 1998)

    Book  Google Scholar 

  2. Martin, P. A., Reimers, T. J., Lodge, J. R. & Dziuk, P. J. The effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. J. Reprod. Fertil. 39, 251–258 (1974)

    CAS  Article  Google Scholar 

  3. Wedell, N., Gage, M. J. W. & Parker, G. A. Sperm competition, male prudence and sperm-limited females. Trends Ecol. Evol. 17, 313–320 (2002)

    Article  Google Scholar 

  4. Pilastro, A., Scaggiante, M. & Rasotto, M. B. Individual adjustment of sperm expenditure accords with sperm competition theory. Proc. Natl Acad. Sci. USA 99, 9913–9915 (2002)

    ADS  CAS  Article  Google Scholar 

  5. Evans, J. P., Pierotti, M. & Pilastro, A. Male mating behavior and ejaculate expenditure under sperm competition risk in the eastern mosquitofish. Behav. Ecol. 14, 268–273 (2003)

    Article  Google Scholar 

  6. Dewsbury, D. A. Ejaculate cost and male choice. Am. Nat. 119, 601–610 (1982)

    Article  Google Scholar 

  7. Pitnick, S. & Markow, T. A. Male gametic strategies: sperm size, testes size, and the allocation of ejaculate among successive mates by the sperm-limited fly Drosophila pachea and its relatives. Am. Nat. 143, 785–819 (1994)

    Article  Google Scholar 

  8. Reinhold, K., Kurtz, J. & Engqvist, L. Cryptic male choice: sperm allocation strategies when female quality varies. J. Evol. Biol. 15, 201–209 (2002)

    Article  Google Scholar 

  9. Pizzari, T. & Birkhead, T. R. Female feral fowl eject sperm of subdominant males. Nature 405, 787 (2000)

    ADS  CAS  Article  Google Scholar 

  10. Pizzari, T. Indirect partner choice through manipulation of male behaviour by female fowl, Gallus g. domesticus. Proc. R. Soc. Lond. B 268, 181–186 (2001)

    CAS  Article  Google Scholar 

  11. Parker, J. E., McKenzie, F. F. & Kempster, H. L. Fertility in the domestic fowl. Miss. Agric. Exp. Station Res. Bull. 347, 3–50 (1942)

    Google Scholar 

  12. Birkhead, T. R., Pellatt, J. E. & Hunter, F. M. Extra-pair copulation and sperm competition in the zebra finch. Nature 334, 60–62 (1988)

    ADS  CAS  Article  Google Scholar 

  13. Westneat, D. F., McGraw, L. A., Fraterrigo, J. M., Birkhead, T. R. & Fletcher, F. Patterns of courtship behavior and ejaculate characteristics in male red-winged blackbirds. Behav. Ecol. Sociobiol. 43, 161–171 (1988)

    Article  Google Scholar 

  14. Hunter, F. M., Harcourt, R., Wright, M. & Davis, L. S. Strategic allocation of ejaculates by male Adélie penguins. Proc. R. Soc. Lond. B 267, 1541–1545 (2000)

    CAS  Article  Google Scholar 

  15. Fumihito, A. et al. Monophyletic origin and unique dispersal patterns of domestic fowls. Proc. Natl Acad. Sci. USA 93, 6792–6795 (1996)

    ADS  CAS  Article  Google Scholar 

  16. Der, G. & Everitt, B. S. A Handbook of Statistical Analyses using SAS 2nd edn (Chapman & Hall, Boca Raton, FL, 2001)

    MATH  Google Scholar 

  17. Pizzari, T. Food, vigilance and sperm: the role of male direct benefits in the evolution of female preference in a polygamous bird. Behav. Ecol. (in the press)

  18. Wilson, J. R., Kuehn, R. E. & Beach, F. A. Modification in the sexual behavior of male rats produced by changing the stimulus female. J. Comp. Physiol. Psycol. 56, 636–644 (1963)

    CAS  Article  Google Scholar 

  19. Pizzari, T. Sperm allocation, the Coolidge effect and female polyandry. Trends Ecol. Evol. 17, 456 (2002)

    Article  Google Scholar 

  20. Zuk, M., Johnsen, T. S. & Maclarty, T. Endocrine–immune interactions, ornaments and mate choice in red jungle fowl. Proc. R. Soc. Lond. B 260, 205–210 (1995)

    ADS  Article  Google Scholar 

  21. Schütz, K. E. & Jensen, P. Effects of resource allocation on behavioural strategies: a comparison of red jungle fowl (Gallus gallus) and two domesticated breeds of poultry. Ethology 107, 753–765 (2001)

    Article  Google Scholar 

  22. Pizzari, T. & Birkhead, T. R. For whom does the hen cackle? The adaptive significance of the post-oviposition cackling. Anim. Behav. 61, 601–607 (2001)

    Article  Google Scholar 

  23. Ishikawa, H. The life duration of cock spermatozoa outside the body. Proc. World Poult. Fourth Congr. 90–94 (1930)

  24. Bakst, M. R. & Cecil, H. C. (eds) Techniques for Semen Evaluation, Semen Storage, and Fertility Determination (Poultry Science Association, Savoy, IL, 1997)

  25. Clutton-Brock, T. H., Albon, S. D., Gibson, R. M. & Guinness, F. E. The logical stag. Anim. Behav. 27, 211–225 (1979)

    Article  Google Scholar 

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Acknowledgements

We thank A. Donald for help with sperm counting, and A. MacColl for statistical advice. T.P. was supported by a scholarship from the Swedish University of Agricultural Sciences and a grant from the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS); T.R.B. by a grant from the Natural Research Council (NERC); C.K.C. by a studentship from NERC (to T.R.B.); and H.L. by a studentship from the Zoology Department of Stockholm University. T.R.B. and T.P. developed the sperm collection technique; T.P. designed the female promiscuity and female novelty experiments, and together with C.K.C. and H.L. carried them out; C.K.C. designed the female quality experiment with T.R.B. and carried it out together with H.L.; C.K.C. analysed the data with T.P.; T.P. wrote the paper; S.J. helped with field work and the provision of research facilities.

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Correspondence to Tommaso Pizzari.

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Pizzari, T., Cornwallis, C., Løvlie, H. et al. Sophisticated sperm allocation in male fowl. Nature 426, 70–74 (2003). https://doi.org/10.1038/nature02004

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