Abstract
A growing amount of experimental data indicates extremely rapid evolution of traits and proteins related to fertilization in many diverging taxa1,2,3. These data come from studies of sperm or pollen competition between closely related species3,4,5,6, and from molecular studies of fertilization proteins2,7,8,9,10. The positive selection for evolutionary novelty that appears to be acting on fertilization systems seems paradoxical because successful reproduction requires the close matching of female and male traits. It has been suggested11,12,13 that perpetual coevolution between the sexes can result from sexual conflict in mating. Sexual conflict occurs when characteristics that enhance the reproductive success of one sex reduce the fitness of the other sex14. Numerous examples of sexual conflict resulting from sensory exploitation, polyspermy and the cost of mating have been discussed in detail1,2,3,14,15. The potential for coevolution due to such conflict has been evaluated experimentally15,16. Here I develop a simple mathematical model describing coevolutionary dynamics of male and female traits involved in reproduction. The model shows that continual change in such traits at a constant speed is expected whenever females (or eggs) experience fitness loss from having too many compatible males (or sperms). The plausibility of runaway coevolution increases with increasing population size. Rapid evolution of reproductive barriers driven by sexual conflict may explain increased speciation rates after colonization of new habitats (‘adaptive radiation’) and high species richness in resource-rich environments.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Turning the tide on sex and the microbiota in aquatic animals
Hydrobiologia Open Access 05 May 2022
-
Juvenile diet quality and intensity of sexual conflict in the mite Sancassania berlesei
BMC Evolutionary Biology Open Access 12 March 2020
-
Molecular evolution of mammalian genes with epistatic interactions in fertilization
BMC Evolutionary Biology Open Access 25 July 2019
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Get just this article for as long as you need it
$39.95
Prices may be subject to local taxes which are calculated during checkout


References
Rice, W. R. in Endless Forms. Species and Speciation (eds Howard, D. J. & Berlocher, S. H.) 261–270 (Oxford Univ. Press, New York, 1998).
Palumbi, S. R. in Endless Forms. Species and Speciation (eds Howard, D. J. & Berlocher, S. H.) 271–278 (Oxford Univ. Press, New York, 1998).
Howard, D. J., Reece, M., Gregory, P. G., Chu, J. & Cain, M. L. in Endless Forms. Species and Speciation (eds Howard, D. J. & Berlocher, S. H.) 279– 288 (Oxford Univ. Press, New York, 1998).
Arnold, M. L., Hamrick, J. L. & Bennett, B. D. Interspecific pollen competition and reproductive isolation in Iris. J. Hered. 84, 13–16 (1993).
Wade, M. J., Patterson, H., Chang, N. W. & Johnson, N. A. Postcopulatory, prezygotic isolation in flour beetles. Heredity 72, 163–167 ( 1994).
Rieseberg, L. H., Desrochers, A. M. & Youn, S. J. Interspecific pollen competition as a reproductive barrier between sympatric species of Helianthus (Asteraceae). Am. J. Bot. 82, 515–519 (1995).
Aguade, M., Miyashita, N. & Langley, C. H. Polymorphism and divergence of the mst 355 male accessory gland region. Genetics 132, 755– 770 (1992).
Palumbi, S. R. Marine speciation on a small planet. Trends Ecol. Evol. 7, 114–117 (1992).
Vacquire, V. D. & Lee, Y.-H. Abalone sperm lysin: unusual mode of evolution of a gamete recognition protein. Zygote 1, 181–196 ( 1993).
Metz, E. C. & Palumbi, S. R. Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. Mol. Biol. Evol. 13, 397– 406 (1996).
Rice, W. R. & Holland, B. The enemies within: intergenomic conflict, interlocus contest evolution (ICE) and the intraspecific red queen. Behav. Ecol. Sociobiol. 41, 1– 10 (1997).
Holland, B. & Rice, W. R. Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52, 1–7 (1998).
Parker, G. A. & Partridge, L. Sexual conflict and speciation. Phil. Trans. R. Soc. Lond. B 353, 261– 274 (1998).
Stockley, P. Sexual conflict resulting from adaptations to sperm competition. Trends Ecol. Evol. 12, 154–159 (1997).
Rice, W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381, 232– 234 (1996).
Holland, B. & Rice, W. R. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc. Natl Acad. Sci. USA 96, 5083– 5088.
Lande, R. Models of speciation by sexual selection on polygenic characters. Proc. Natl Acad. Sci. USA 78, 3721– 3725 (1981).
Arnqvist, G. & Nilson, T. The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. (submitted).
Iwasa, I. & Pomiankowski, A. Continual change in mate preferences. Nature 377, 420–422 (1995).
Gavrilets, S. Coevolutionary chase in exploiter–victim systems with polygenic characters. J. Theor. Biol. 186, 527– 534 (1997).
Barton, N. H. & Turelli, M. Natural and sexual selection on many loci. Genetics 127, 229– 255 (1991).
Gavrilets, S. & Hastings, A. Dynamics of polygenic variability under stabilizing selection, recombination and drift. Genet. Res. 65, 63–74 ( 1995).
Arnqvist, G., Edvardsson, M., Friberg, U. & Nilsson, T. Sexual conflict promotes speciation in insects. Proc. R. Soc. Lond. B (submitted).
Walsh, J. B. Rate of accumulation of reproductive isolation by chromosome rearrangements. Am. Nat. 120, 510–532 (1982).
Gavrilets, S. Evolution and speciation on holey adaptive landscapes. Trends Ecol. Evol. 12, 307–312 ( 1997).
Gavrilets, S. A dynamical theory of speciation on holey adaptive landscapes. Am. Nat. 154, 1–22 ( 1999).
Arnqvist, G. in The Evolution of Mating Systems in Insects and Arachnids (eds Choe, J. C. & Crespi, B. J.) 146–163 (Cambridge Univ. Press, Cambridge, Massachusetts, 1997).
Schluter, D. in Endless Forms. Species and Speciation (eds Howard, D. J. & Berlocher, S. H.) 114–129 (Oxford Univ. Press, New York, 1998).
Rosenzweig, M. L. Species Diversity in Space and Time (Cambridge Univ. Press, Cambridge, Massachusetts, 1995).
Bürger, R. & Lynch, M. Evolution and extinction in a changing environment—a quantitative genetic analysis. Evolution 49, 151–163.
Acknowledgements
I am grateful to G. Arnqvist, C. R. B. Boake, M. B. Cruzan and G. McCracken for discussions and/or helpful comments on the manuscript. This work was supported by an NIH grant and by a grant from the Netherlands Organization for Scientific Research (NWO).
Author information
Authors and Affiliations
Corresponding author
Supplementary Information
Rights and permissions
About this article
Cite this article
Gavrilets, S. Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403, 886–889 (2000). https://doi.org/10.1038/35002564
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/35002564
This article is cited by
-
Turning the tide on sex and the microbiota in aquatic animals
Hydrobiologia (2022)
-
Juvenile diet quality and intensity of sexual conflict in the mite Sancassania berlesei
BMC Evolutionary Biology (2020)
-
Molecular evolution of mammalian genes with epistatic interactions in fertilization
BMC Evolutionary Biology (2019)
-
Meta-analytic evidence that sexual selection improves population fitness
Nature Communications (2019)
-
Who determines the timing of inflorescence closure of a sexual dandelion? Pollen donors versus recipients
Evolutionary Ecology (2019)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.