The evolution of reproductive isolation through sexual conflict

Abstract

Classical population-genetics theory suggests that reproductive isolation will evolve fastest in small isolated populations1. In contrast, recent theory suggests that divergence should occur fastest in larger allopatric populations2. The rationale behind this is that sexual conflict, potentially the strongest driver of speciation, is greater in larger, higher-density populations. This idea is highly controversial3 and has little experimental support4,5. Here we show, using replicate fly populations with varying levels of sexual conflict, that larger, more dense populations with more sexual conflict diverged to a greater degree than small populations with relaxed conflict. This result strongly suggests that speciation can occur rapidly in large populations through increased sexual conflict.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Interaction plot showing the effects of treatment (monogamy, low-density or high-density populations) and mating type (within populations or between populations of the same treatment) on the proportion of pairs that copulated.
Figure 2: Interaction plot showing the effects of treatment (monogamy, low-density or high-density populations) and mating type (within populations or between populations of the same treatment) on female reluctance (reluctance to mate is stereotypical and violent shaking behaviour).

References

  1. 1

    Lande, R. Models of speciation by sexual selection on polygenic characters. Proc. Natl Acad. Sci. USA 78, 3721–3725 (1981)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Gavrilets, S. Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403, 886–889 (2000)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Tregenza, T., Butlin, R. K. & Wedell, N. Sexual conflict and speciation. Nature 407, 149–150 (2000)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Rice, W. R. & Hostert, E. E. Laboratory experiments on speciation: what have we learned in 40 years? Evolution 47, 1637–1653 (1993)

    Article  Google Scholar 

  5. 5

    Price, T. Sexual selection and natural selection in bird speciation. Phil. Trans. R. Soc. Lond. B 353, 251–260 (1998)

    Article  Google Scholar 

  6. 6

    Parker, G. A. in Sexual Selection and Reproductive Competition in Insects (eds Blum, M. S. & Blum, N. B.) 123–166 (Academic, New York, 1979)

    Google Scholar 

  7. 7

    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)

    Article  Google Scholar 

  8. 8

    Swanson, W. J. & Vacquier, V. D. The rapid evolution of reproductive proteins. Nature Rev. Genet. 3, 137–144 (2002)

    CAS  Article  Google Scholar 

  9. 9

    Rice, W. R. in Endless Forms: Species and Speciation (eds Howard, D. J. & Berlocher, S. H.) 261–270 (Oxford Univ. Press, New York, 1998)

    Google Scholar 

  10. 10

    Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, Oxford, 2000)

    Google Scholar 

  11. 11

    Rice, W. R. Dangerous liaisons. Proc. Natl Acad. Sci. USA 98, 12953–12955 (2000)

    ADS  Article  Google Scholar 

  12. 12

    Arnqvist, G., Edvardsson, M., Friberg, U. & Nilsson, T. Sexual conflict promotes speciation in insects. Proc. Natl Acad. Sci. USA 97, 10460–10464 (2000)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Gage, M. J. G., Parker, G. A., Nylin, S. & Wiklund, C. Sexual selection and speciation in mammals, butterflies and spiders. Proc. R. Soc. Lond. B 269, 2309–2316 (2002)

    Article  Google Scholar 

  14. 14

    Sharp, P. M. The effect of inbreeding on competitive male-mating ability in Drosophila melanogaster. Genetics 106, 601–612 (1984)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. 15

    Meffert, L. M. & Bryant, E. H. Mating propensity and courtship behavior in serially bottlenecked lines of the housefly. Evolution 45, 293–306 (1991)

    Article  Google Scholar 

  16. 16

    Meffert, L. M. & Bryant, E. H. Divergent ambulatory and grooming behavior in serially bottlenecked lines of the housefly. Evolution 46, 1399–1407 (1992)

    Article  Google Scholar 

  17. 17

    Cooper, T. F., Rozen, D. E. & Lenski, R. E. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc. Natl Acad. Sci. USA 100, 1072–1077 (2003)

    ADS  CAS  Article  Google Scholar 

  18. 18

    Andrés, J. A. & Morrow, E. H. The origin of interlocus sexual conflict: is sex linkage important? J. Evol. Biol. 16, 219–223 (2003)

    Article  Google Scholar 

  19. 19

    Parker, G. A. Reproductive behaviour of Sepsis cynipsea (L.) (Diptera: Sepsidae) I. A preliminary analysis of the reproductive strategy and its associated behaviour patterns. Behaviour 41, 172–206 (1972)

    Article  Google Scholar 

  20. 20

    Parker, G. A. Reproductive behaviour of Sepsis cynipsea (L.) (Diptera: Sepsidae) II. The significance of the precopulatory passive phase and emigration. Behaviour 41, 242–250 (1972)

    Article  Google Scholar 

  21. 21

    Ward, P. I., Hemmi, J. & Röösli, T. Sexual conflict in the dung fly Sepsis cynipsea. Funct. Ecol. 6, 649–653 (1992)

    Article  Google Scholar 

  22. 22

    Blanckenhorn, W. U. et al. The costs of copulating in the dung fly Sepsis cynipsea. Behav. Ecol. 13, 353–358 (2002)

    Article  Google Scholar 

  23. 23

    Martin, O. Y. & Hosken, D. J. Strategic ejaculation in the common dung fly Sepsis cynipsea. Anim. Behav. 63, 541–546 (2002)

    Article  Google Scholar 

  24. 24

    Martin, O. Y., Leugger, R. R., Zeltner, N. & Hosken, D. J. Male age, mating probability and mating costs in the fly Sepsis cynipsea. Evol. Ecol. Res. 5, 119–129 (2003)

    Google Scholar 

  25. 25

    Blanckenhorn, W. U., Mühlhäuser, C., Morf, C., Reusch, T. & Reuter, M. Female choice, female reluctance to mate and sexual selection on body size in the dung fly Sepsis cynipsea. Ethology 106, 577–593 (2000)

    Article  Google Scholar 

  26. 26

    Hosken, D. J., Martin, O. Y., Born, J. & Huber, F. Sexual conflict in Sepsis cynipsea: female reluctance, fertility and mate choice. J. Evol. Biol. 16, 485–490 (2003)

    CAS  Article  Google Scholar 

  27. 27

    Mühlhäuser, C. & Blanckenhorn, W. U. The costs of avoiding matings in the dung fly Sepsis cynipsea. Behav. Ecol. 13, 359–365 (2002)

    Article  Google Scholar 

  28. 28

    Ding, A. & Blanckenhorn, W. U. The effect of sexual size dimorphism on mating behaviour in two dung flies with contrasting dimorphism. Evol. Ecol. Res. 4, 259–273 (2002)

    Google Scholar 

Download references

Acknowledgements

We thank the SNF for financial support, and R. Leugger, K. Landergott and M. Eger for laboratory help. We also thank W. Blanckenhorn for statistical advice, F. Balloux for comments on the experimental design, and G. Arnqvist, A. Badyaev, F. Balloux, P. Bauerfeind, J. Evans, T. Garner, B. Holland, L. Keller, T. Pizzari and L. Simmons for valuable comments on this manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Oliver Y. Martin.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Martin, O., Hosken, D. The evolution of reproductive isolation through sexual conflict. Nature 423, 979–982 (2003). https://doi.org/10.1038/nature01752

Download citation

Further reading

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.

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing