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Sperm competition between Drosophila males involves both displacement and incapacitation

Abstract

Females in almost all animal groups copulate with multiple males1,2. This behaviour allows different males to compete for fertilization3 and gives females the opportunity to mediate this competition4. In many animals and most insects, the second male to copulate with a female typically sires most of her offspring1,5,6. In Drosophila melanogaster, this second-male sperm precedence has long been studied7,8,9,10,11,12,13,14,15 but, as in most species, its mechanism has remained unknown. Here we show, using labelled sperm in doubly mated females, that males can both physically displace andincapacitate stored sperm from earlier-mating males. Displacement occurs only if the second male transfers sperm to the female, and in only one of her three sperm-storage organs. Incapacitation can be caused by either fertile or spermless second males, but requires extended intervals between matings. Sperm from different males are not ‘stratified’ in the storage organs but mix freely. Many animal species may have multiple mechanisms of sperm competition like those observed here, and revealing these mechanisms is necessary to understand the genetic and evolutionary basis of second-male sperm precedence in animals.

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Figure 1: The mechanism of sperm competition depends on mating interval.
Figure 2: Differentially labelled sperm.
Figure 3: Physical displacement of first-male sperm.

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References

  1. Smith, R. L. (ed.) Sperm Competition and the Evolution of Animal Mating Systems (Academic, London, (1984).

    Google Scholar 

  2. Birkhead, T. R. & Møller, A. P. (eds.) Sperm Competition and Sexual Selection (Academic, London, (1998).

    Google Scholar 

  3. Parker, G. A. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525–567 (1970).

    Article  Google Scholar 

  4. Eberhard, W. G. Female Control: Sexual Selection by Cryptic Female Choice (Princeton Univ. Press, Princeton, (1996).

    Google Scholar 

  5. Birkhead, T. R. & Møller, A. P. Sperm Competition in Birds: Evolutionary Causes and Consequences (Academic, London, (1992).

    Google Scholar 

  6. Simmons, L. W. & Siva-Jothy, M. T. in Sperm Competition and Sexual Selection (eds Birkhead, T. R. & Møller, A. P.) 341–434 (Academic, London, (1998).

    Book  Google Scholar 

  7. Nonidez, J. F. The internal phenomena of reproduction in Drosophila. Biol. Bull. 39, 207–230 (1920).

    Article  Google Scholar 

  8. Lobashov, M. E. Mixture of sperm in case of polyandry in Drosophila melanogaster. C. R. (Doklady) Acad. Sci. de l'URSS 23, 827–830 (1939).

    Google Scholar 

  9. Kaufmann, B. P. & Demerec, M. Utilization of sperm by the female Drosophila melanogaster. Am. Nat. 76, 445–469 (1942).

    Article  Google Scholar 

  10. Lefevre, G. & Jonsson, U. B. Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics 47, 1719–1736 (1962).

    PubMed  PubMed Central  Google Scholar 

  11. Newport, M. E. A. & Gromko, M. H. The effect of experimental design on female receptivity to remating and its impact on reproductive success in Drosophila melanogaster. Evolution 38, 1261–1272 (1984).

    Article  Google Scholar 

  12. Scott, D. & Richmond, R. C. Sperm loss by remating Drosophila melanogaster females. J. Insect Physiol. 36, 451–456 (1990).

    Article  Google Scholar 

  13. Scott, D. & Williams, E. Sperm displacement after remating in Drosophila melanogaster. J. Insect Physiol. 39, 201–206 (1993).

    Article  Google Scholar 

  14. Harshman, L. G. & Prout, T. Sperm displacement without sperm transfer in Drosophila melanogaster. Evolution 48, 758–766 (1994).

    Article  Google Scholar 

  15. Gilchrist, A. S. & Partridge, L. Male identity and sperm displacement in Drosophila melanogaster. J. Insect Physiol. 41, 1087–1092 (1995).

    Article  CAS  Google Scholar 

  16. Gromko, M. H., Gilbert, D. G. & Richmond, R. C. in Sperm Competition and the Evolution of Animal Mating Systems (ed. Smith, R. L.) 371–426 (Academic, London, (1984).

    Book  Google Scholar 

  17. Imhof, M., Harr, B., Brem, G. & Schlötterer, C. Multiple mating in wild Drosophila melanogaster revisited by microsatellite analysis. Mol. Ecol. 7, 915–917 (1998).

    Article  CAS  Google Scholar 

  18. Gromko, M. H. & Markow, T. A. Courtship and remating in field populations of Drosophila. Anim. Behav. 45, 253–262 (1993).

    Article  Google Scholar 

  19. Gromko, M. H., Newport, M. E. A. & Kortier, M. G. Sperm dependence of female receptivity to remating in Drosophila melanogaster. Evolution 38, 1273–1282 (1984).

    Article  Google Scholar 

  20. Santel, A., Winhauer, T., Blümer, N. & Renkawitz-Pohl, R. The Drosophila don juan (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of a repetitive amino acid motif. Mech. Dev. 64, 19–30 (1997).

    Article  CAS  Google Scholar 

  21. Snedecor, G. W. & Cochran, W. G. Statistical Methods (Iowa State Univ. Press, Ames, (1967).

    MATH  Google Scholar 

  22. Sokal, R. R. & Rohlf, F. J. Biometry (Freeman, New York, (1995).

    MATH  Google Scholar 

  23. Nachtsheim, H. Eine Method zur Prüfung der Lebendauer genotypisch verschiedener Spermien bei Drosophila. Verhandl. V. Intern. Kongr. Verebungsw., 1143–1147. Z. Ind. Abst. Vereb (Suppl. II) (1927).

  24. Rice, W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381, 232–234 (1996).

    Article  ADS  CAS  Google Scholar 

  25. Clark, A. G. & Begun, D. J. Female genotypes affect sperm displacement in Drosophila. Genetics 149, 1487–1493 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Clark, A. G., Begun, D. J. & Prout, T. Female × male interactions in Drosophila sperm competition. Science 283, 217–220 (1999).

    Article  CAS  Google Scholar 

  27. Price, C. S. C. Conspecific sperm precedence in Drosophila. Nature 388, 663–666 (1997).

    Article  ADS  CAS  Google Scholar 

  28. Coyne, J. A., Aulard, S. & Berry, A. Lack of underdominance in a naturally occurring pericentric inversion in Drosophila melanogaster and its implications for chromosome evolution. Genetics 129, 791–802 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Ingman-Baker, J. & Candido, E. P. Proteins of the Drosophila melanogaster male reproductive system: two-dimensional gel patterns of proteins synthesized in the XO, XY, and XYY testis and paragonial gland and evidence that the Y chromosome does not code for structural sperm proteins. Biochem. Genet. 18, 809–828 (1980).

    Article  CAS  Google Scholar 

  30. Kiefer, B. I. Ultrastructural abnormalities in developing sperm of X/O Drosophila melanogaster. Genetics 54, 14441–1452 (1966).

    Google Scholar 

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Acknowledgements

We thank M. DeAngelis, C. Gronlund, C. Kim, C. Mercader, J. Posluszny and A.Travelli for technical assistance; A. Santel for the dj GFP II/Cyo flies; A. James and R. Snook for miscellaneous help; B. Robbins for supplies; and A. Civetta, T. Prout and C.-I. Wu for comments. This work was supported by an NSF predoctoral fellowship, NIH genetics training grant and NSF doctoral dissertation improvement grant to C.S.C.P. and by an NIH grant to J.A.C.

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Correspondence to Jerry A. Coyne.

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Price, C., Dyer, K. & Coyne, J. Sperm competition between Drosophila males involves both displacement and incapacitation. Nature 400, 449–452 (1999). https://doi.org/10.1038/22755

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