Comparative evidence for the evolution of genitalia by sexual selection

Abstract

Rapid divergent evolution of male genitalia is one of the most general evolutionary trends in animals with internal fertilization; the shapes of genital traits often provide the only reliable characters for species identification1. Yet the evolutionary processes responsible for this pattern remain obscure. The long-standing lock-and-key hypothesis, still popular among taxonomists, suggests that genitalia evolve by pre-insemination hybridization avoidance; that is, hybrid inferiority drives the evolution of male genitalia with a proper mechanical fit to female genitalia. The sexual selection hypothesis2,3, in contrast, proposes that divergent evolution of genitalia is the result of sexual selection, brought about by variation in postinsemination paternity success among males. Here, by comparing pairs of related clades of insects that differ in mating system, I assess how the opportunity for postmating sexual selection affects the rate of divergent evolution of male genitalia. Genital evolution is more than twice as divergent in groups in which females mate several times than in groups in which females mate only once. This pattern is not found for other morphological traits. These findings provide strong empirical evidence in favour of a postmating sexual selection mechanism of genital evolution.

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: Comparison of the rate of genitalic evolution in polyandrous and monandrous clades.

References

  1. 1

    Eberghard, W. G. Sexual Selection and Animal Genitalia(Harvard Univ. Press, Cambridge, MA, 1985).

    Google Scholar 

  2. 2

    Eberhard, W. G. Evaluating models of sexual selection: genitalia as a test case. Am. Nat. 142, 564–571 (1993).

    CAS  Article  Google Scholar 

  3. 3

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

    Google Scholar 

  4. 4

    Lloyd, J. E. Mating behavior and natural selection. Fla. Entomol. 62, 17–34 (1979).

    Article  Google Scholar 

  5. 5

    Thornhill, R. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. Am. Nat. 122, 765–788 (1983).

    Article  Google Scholar 

  6. 6

    Waage, J. K. Dual function of the damselfly penis: sperm removal and transfer. Science 203, 916–918 (1979).

    ADS  CAS  Article  Google Scholar 

  7. 7

    Gage, M. J. Removal of rival sperm during copulation in a beetle, Tenebrio molitor. Anim. Behav. 44, 587–589 (1992).

    Article  Google Scholar 

  8. 8

    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 

  9. 9

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

    ADS  CAS  Article  Google Scholar 

  10. 10

    Alexander, R. D., Marshall, D. C. & Cooley, J. R. in The Evolution of Mating Systems in Insects and Arachnids(eds Choe, J. C. & Crespi, B. J.) 4–31 (Cambridge Univ. Press 1997).

    Google Scholar 

  11. 11

    Verell, P. A. Primate penile morphologies and social systems: further evidence for an association. Folia Primatol. (Basel) 59, 114–120 (1992).

    Article  Google Scholar 

  12. 12

    Harcourt, A. H. & Gardiner, J. Sexual selection and genital anatomy of male primates. Proc. R. Soc. Lond. B 255, 47–53 (1994).

    ADS  CAS  Article  Google Scholar 

  13. 13

    Proctor, H. C., Baker, R. L. & Gwynne, D. T. Mating behaviour and spermatophore morphology: a comparative test of the female-choice hypothesis. Can. J. Zool. 73, 2010–2020 (1995).

    Article  Google Scholar 

  14. 14

    Lestrel, P. E. (ed) Fourier Descriptors and their Applications in Biology(Cambridge Univ. Press, 1997).

    Google Scholar 

  15. 15

    Rohlf, F. J. in Ordination in the Study of Morphology, Evolution and Systematics of Insects(eds Sorensen, J. T. & Foottit, R.) 95–112 (Elsevier, Amsterdam, 1992).

    Google Scholar 

  16. 16

    Arnqvist, G. The evolution of animal genitalia: distinguishing between hypotheses by single species studies. Biol. J. Linn. Soc. 60, 365–379 (1997).

    Article  Google Scholar 

  17. 17

    Darwin, C. The Descent of Man, and Selection in Relation to Sex(Murray, London, 1871).

    Google Scholar 

  18. 18

    Andersson, M. Sexual Selection(Princeton Univ. Press, Princeton, NJ, 1994).

    Google Scholar 

  19. 19

    Pomiankowski, A. & Møller, A. P. Aresolution of the lek paradox. Proc. R. Soc. Lond. B 260, 21–29 (1995).

    ADS  Article  Google Scholar 

  20. 20

    Rowe, L. & Houle, D. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. B 263, 1415–1421 (1996).

    ADS  Article  Google Scholar 

  21. 21

    Burt, A. Comparative methods using phylogenetically independent contrasts. Oxf. Surv. Evol. Biol. 6, 33–53 (1989).

    Google Scholar 

  22. 22

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

    Google Scholar 

  23. 23

    Thornhill, R. & Alcock, J. The Evolution of Insect Mating Systems(Harvard Univ. Press, Cambridge, MA, 1983).

    Google Scholar 

  24. 24

    Ridley, M. The timing and frequency of mating in insects. Anim. Behav. 37, 535–545 (1989).

    Article  Google Scholar 

  25. 25

    Ridley, M. The incidence of sperm displacement in insects: four conjectures, one corroboration. Biol. J. Linn. Soc. 38, 349–367 (1989).

    Article  Google Scholar 

  26. 26

    Ridley, M. The control and frequency of mating in insects. Funct. Ecol. 4, 75–84 (1990).

    Article  Google Scholar 

  27. 27

    Ferson, S., Rohlf, F. J. & Koehn, R. K. Measuring shape variation of two-dimensional outlines. Syst. Zool. 34, 59–68 (1985).

    Article  Google Scholar 

  28. 28

    Rohlf, F. J. & Archie, J. Acomparison of Fourier methods for the description of wing shape in mosquitoes (Diptera: Culicidae). Syst. Zool. 33, 302–317 (1984).

    Article  Google Scholar 

  29. 29

    Liu, J. et al. Genetic analysis of a morphological shape difference in the male genitalia of Drosophila similans and D. mauritiana. Genetics 142, 1129–1145 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

I thank L. Rowe and P. Watson for comments. This study was made possible by the expert advice from many entomologists (see Supplementary information), and was generously funded by a grant from the Swedish Natural Science Research Council.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Göran Arnqvist.

Supplementary Information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Arnqvist, G. Comparative evidence for the evolution of genitalia by sexual selection. Nature 393, 784–786 (1998). https://doi.org/10.1038/31689

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.