Mating with more than one male is the norm for females of many species. In addition to generating competition between the ejaculates of different males1,2, multiple mating may allow females to bias sperm use3,4. In Drosophila melanogaster, the last male to inseminate a female sires approximately 80% of subsequent progeny5. Both sperm displacement, where resident sperm are removed from storage by the incoming ejaculate of the copulating male6, and sperm incapacitation, where incoming seminal fluids supposedly interfere with resident sperm7, have been implicated in this pattern of sperm use5,6,7,8,9,10,11,12. But the idea of incapacitation is problematic because there are no known mechanisms by which an individual could damage rival sperm and not their own. Females also influence the process of sperm use13,14, but exactly how is unclear. Here we show that seminal fluids do not kill rival sperm and that any ‘incapacitation’ is probably due to sperm ageing during sperm storage. We also show that females release stored sperm from the reproductive tract (sperm dumping) after copulation with a second male and that this requires neither incoming sperm nor seminal fluids. Instead, males may cause stored sperm to be dumped or females may differentially eject sperm from the previous mating.
Access optionsAccess options
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Simmons, L. W. Sperm Competition and its Evolutionary Consequences in the Insects (Princeton Univ. Press, Princeton, 2001)
Parker, G. A. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45, 525–567 (1970)
Eberhard, W. G. Female Control: Sexual Selection by Cryptic Female Choice (Princeton Univ. Press, Princeton, 1996)
Pitnick, S. & Brown, W. D. Criteria for demonstrating female sperm choice. Evolution 54, 1052–1056 (2000)
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)
Lefevre, G. J. & Jonsson, U. B. Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics 47, 1719–1736 (1962)
Harshman, L. G. & Prout, T. Sperm displacement without sperm transfer in Drosophila melanogaster. Evolution 48, 758–766 (1994)
Price, C. S. P., Dyer, K. A. & Coyne, J. A. Sperm competition between Drosophila males involves both displacement and incapacitation. Nature 400, 449–452 (1999)
Civetta, A. Direct visualization of sperm competition and sperm storage in Drosophila. Curr. Biol. 9, 841–844 (1999)
Gilchrist, A. S. & Partridge, L. Male identity and sperm displacement in Drosophila melanogaster. J. Insect Physiol. 41, 1087–1092 (1995)
Scott, D. & Richmond, R. C. Sperm loss by remating Drosophila melanogaster females. J. Insect Physiol. 36, 451–456 (1990)
Gilchrist, A. S. & Partridge, L. Why is it difficult to model sperm displacement in Drosophila melanogaster: the relation between sperm transfer and copulation duration. Evolution 54, 534–542 (2000)
Miller, G. T. & Pitnick, S. Sperm–female coevolution in Drosophila. Science 298, 1230–1233 (2002)
Clark, A. G., Begun, D. J. & Prout, T. Female × male interactions in Drosophila sperm competition. Science 283, 217–220 (1999)
Birkhead, T. R. & Møller, A. P. Sperm Competition and Sexual Selection (Academic, London, 1998)
Simmons, L. W. & Siva-Jothy, M. S. in Sperm Competition and Sexual Selection (eds Birkhead, T. R. & Møller, A. P.) 341–434 (Academic Press, London, 1998)
Moore, H. D. M., Martin, M. & Birkhead, T. R. No evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. Proc. R. Soc. Lond. B 266, 2343–2350 (1999)
Jenzer, B. & Steinmann-Zwicky, M. Cell-autonomous and somatic signals control sex-specific gene expression in XY germ cells of Drosophila. Mech. Dev. 100, 3–13 (2001)
Wheeler, M. R. The insemination reaction in intraspecific matings. Univ. Texas Publ. Genet. 4720, 78–115 (1947)
Heed, W. B. in Genetics, Speciation, and the Founder Principle (eds Giddings, L. V., Kaneshiro, K. Y. & Anderson, W. W.) 253–278 (Oxford Univ. Press, Oxford, 1990)
Alonzo-Pimentel, H., Tolbert, L. P. & Heed, W. B. Ultrastructural examination of the insemination reaction in Drosophila. Cell Tissue Res. 275, 467–479 (1994)
Arthur, B. I., Hauschteck-Jungen, E., Nothiger, R. & Ward, P. I. A female nervous system is necessary for normal sperm storage in Drosophila melanogaster: a masculinized nervous system is as good as none. Proc. R. Soc. Lond. B 265, 1749–1753 (1998)
Xue, L. & Noll, M. Drosophila female sexual behavior induced by sterile males showing copulation complementation. Proc. Natl Acad. Sci. USA 97, 3272–3275 (2000)
Gromko, M. H., Newport, M. A. E. & Kortier, M. G. Sperm dependence of female receptivity to remating in Drosophila melanogaster. Evolution 38, 1273–1282 (1984)
Pizzari, T. & Birkhead, T. R. Female feral fowl eject sperm of subdominant males. Nature 405, 787–789 (2000)
Cordoba-Aguilar, A. Male copulatory sensory stimulation induces female ejection of rival sperm in a damselfly. Proc. R. Soc. Lond. B 266, 779–784 (1999)
Otronen, M. & Siva-Jothy, M. T. The effects of postcopulatory male behaviour on ejaculate distribution within the female sperm storage organs of the fly Dryomyza anilis (Diptera: Dryomyzidae). Behav. Ecol. Sociobiol. 29, 33–37 (1991)
Civetta, A. & Clarke, A. G. Chromosomal effects on male and female components of sperm precedence in Drosophila. Genet. Res. 75, 143–151 (2000)
DeVries, J. K. Insemination and sperm storage in Drosophila melanogaster. Evolution 18, 271–282 (1964)
Hunter, F. M. & Birkhead, T. R. Sperm viability and sperm competition in insects. Curr. Biol. 12, 121–123 (2002)
We thank E. Kubli, J. Peng, Y. Choffat, M. Steinmann-Zwicky, J. Henner, M. Noll and E. Frei for supplying flies. Without the generosity of these people, this project would not have been possible. Further thanks go to Carl Zeiss AG for providing a microscope while we tested the sperm staining technique, to M. Oswald for his technical help, and to the Zoology Museum for support and for financing accommodation for R.R.S. during one visit to Zürich. We also thank T. Birkhead, B. Holland, J. Kotiaho, L. Simmons, M. Siva-Jothy, J. Slate, P. Stockley and T. Tregenza for comments on the work, and W. Blanckenhorn for statistical advice. This work was supported by the SNF (D.J.H.) and the US National Science Foundation (R.R.S.).
The authors declare that they have no competing financial interests.
About this article
Science Advances (2018)
Behavioral Ecology (2018)
Insect Science (2018)
Ecology and Evolution (2018)