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Antagonistic coevolution between the sexes in a group of insects

Abstract

In coevolutionary ‘arms races’ between the sexes, the outcome of antagonistic interactions may remain at an evolutionary standstill. The advantage gained by one sex, with any evolutionary exaggeration of arms, is expected to be matched by analogous counteradaptations in the other sex1,2. This fundamental coevolutionary process may thus be hidden from the evolutionist's eye3,4, and no natural examples are known. We have studied the effects of male and female armament (clasping and anti-clasping morphologies) on the outcome of antagonistic mating interactions in 15 species of water strider, using a combination of experimental and phylogenetic comparative methods. Here we present, by assessing the independent effects of both species-specific level of arms escalation and small imbalances in the amounts of arms between the sexes within species, the consequences of a sexual arms race. Evolutionary change in the balance of armament between males and females, but not in the species-specific level of escalation, has resulted in evolutionary change in the outcome of sexually antagonistic interactions such as mating rate.

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Figure 1: Coevolution of arms in males and females.

References

  1. 1

    Chapman, T. & Partridge, L. Sexual conflict as fuel for evolution. Nature 381, 189–190 (1996).

    ADS  CAS  Article  Google Scholar 

  2. 2

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

    ADS  CAS  Article  Google Scholar 

  3. 3

    Rice, W. R. Dangerous liaisons. Proc. Natl Acad. Sci. USA 97, 12953–12955 (2000).

    ADS  CAS  Article  Google Scholar 

  4. 4

    Partridge, L. & Hurst, L. D. Sex and conflict. Science 281, 2003–2008 (1998).

    CAS  Article  Google Scholar 

  5. 5

    Gavrilets, S., Arnqvist, G. & Friberg, U. The evolution of female mate choice by sexual conflict. Proc. R. Soc. Lond. B 268, 531–539 (2001).

    CAS  Article  Google Scholar 

  6. 6

    Civetta, A. & Clark, A. G. Correlated effects of sperm competition and postmating female mortality. Proc. Natl Acad. Sci. USA 97, 13162–13165 (2000).

    ADS  CAS  Article  Google Scholar 

  7. 7

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

    ADS  CAS  Article  Google Scholar 

  8. 8

    Swanson, W. J., Yang, Z., Wolfner, M. F. & Aquadro, C. F. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc. Natl Acad. Sci. USA 98, 2509–2514 (2001).

    ADS  CAS  Article  Google Scholar 

  9. 9

    Arnqvist, G. Comparative evidence for the evolution of genitalia by sexual selection. Nature 393, 784–786 (1998).

    ADS  CAS  Article  Google Scholar 

  10. 10

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

    Google Scholar 

  11. 11

    Parker, G. A. & Partridge, L. Sexual conflict and speciation. Phil. Trans. R. Soc. Lond. B 353, 261–274 (1998).

    CAS  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

    Parker, G. A. in Sexual Selection and Reproductive Competition in Insects (eds Blum, M. S. & Blum, N. A.) 123–163 (Academic, New York, 1979).

    Google Scholar 

  14. 14

    Parker, G. A. Arms races in evolution—an ESS to the opponent-independent cost game. J. Theor. Biol. 101, 619–648 (1983).

    ADS  Article  Google Scholar 

  15. 15

    Härdling, R. Arms races, conflict costs and evolutionary dynamics. J. Theor. Biol. 196, 163–167 (1999).

    Article  Google Scholar 

  16. 16

    Harvey, P. H. & Pagel, M. D. The Comparative Method in Evolutionary Biology (Oxford Univ. Press, Oxford, 1991).

    Google Scholar 

  17. 17

    Garland, T., Harvey, P. H. & Ives, A. R. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18–32 (1992).

    Article  Google Scholar 

  18. 18

    Rowe, L., Arnqvist, G., Sih, A. & Krupa, J. J. Sexual conflict and the evolutionary ecology of mating patterns: water striders as a model system. Trends Ecol. Evol. 9, 289–293 (1994).

    CAS  Article  Google Scholar 

  19. 19

    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, 1997).

    Book  Google Scholar 

  20. 20

    Arnqvist, G. & Rowe, L. Correlated evolution of male and female morphologies in water striders. Evolution (in the press).

  21. 21

    Arnqvist, G. Sexual selection in water strider: the function, nature of selection and heritability of a male grasping apparatus. Oikos 56, 344–350 (1989).

    Article  Google Scholar 

  22. 22

    Arnqvist, G. & Rowe, L. Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proc. R. Soc. Lond. B 261, 123–127 (1995).

    ADS  Article  Google Scholar 

  23. 23

    Losos, J. B. Uncertainty in the reconstruction of ancestral character states and limitations on the use of phylogenetic comparative methods. Anim. Behav. 58, 1319–1324 (1999).

    CAS  Article  Google Scholar 

  24. 24

    Gittleman, J. L. & Kot, M. Adaptation—statistics and a null model for estimating phylogenetic effects. Syst. Zool. 39, 227–241 (1990).

    Article  Google Scholar 

  25. 25

    Rowe, L. 1994. The costs of mating and mate choice in water striders. Anim. Behav. 48, 1049–1056 (1994).

    Article  Google Scholar 

  26. 26

    Watson, P. J., Arnqvist, G. & Stallman, R. R. Sexual conflict and the energetic costs of mating and mate choice in water striders. Am. Nat. 151, 46–58 (1998).

    CAS  Article  Google Scholar 

  27. 27

    Felsenstein, J. The Phylogeny Inference Package [online]. 〈http://evolution.genetics.washington.edu/phylip.html〉 (2001).

  28. 28

    Damgaard, J. & Sperling, F. A. H. Phylogeny of the water strider genus Gerris Fabricius (Heteroptera : Gerridae) based on COI mtDNA, EF-1α nuclear DNA and morphology. Syst. Entomol. 26, 241–254 (2001).

    Article  Google Scholar 

  29. 29

    Rohlf, F. J. & Corti, M. Use of two-block partial least-squares to study covariation in shape. Syst. Biol. 49, 740–753 (2000).

    CAS  Article  Google Scholar 

  30. 30

    Rowe, L. & Arnqvist, G. Sexually antagonistic coevolution in a mating system: combining comparative and experimental approaches to address evolutionary process. Evolution (in the press).

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Acknowledgements

This study was supported by the Swedish Natural Science Research Council, the Natural Sciences and Engineering Research Council of Canada, the Swedish Foundation for International Cooperation in Research and Higher Education, the Knut and Alice Wallenberg Foundation and the Magnus Bergvalls Stiftelse. We thank N. M. Andersen and J. Damgaard for phylogenetic information; J. Felsenstein and F. J. Rohlf for developing software; and T. Day, U. Friberg, D. Schluter and T. Tregenza for comments.

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Correspondence to Göran Arnqvist.

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Arnqvist, G., Rowe, L. Antagonistic coevolution between the sexes in a group of insects. Nature 415, 787–789 (2002). https://doi.org/10.1038/415787a

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