Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 Oct 7;270(1528):2009–2016. doi: 10.1098/rspb.2003.2453

Detecting sexually antagonistic coevolution with population crosses.

Locke Rowe 1, Erin Cameron 1, Troy Day 1
PMCID: PMC1691476  PMID: 14561288

Abstract

The result of population crosses on traits such as mating rate, oviposition rate and survivorship are increasingly used to distinguish between modes of coevolution between the sexes. Two key hypotheses, erected from a verbal theory of sexually antagonistic coevolution, have been the subject of several recent tests. First, statistical interactions arising in population crosses are suggested to be indicative of a complex signal/receiver system. In the case of oviposition rates, an interaction between populations (x, y and z) would be indicated by the rank order of female oviposition rates achieved by x, y and z males changing depending upon the female (x, y or z) with which they mated. Second, under sexually antagonistic coevolution females will do 'best' when mated with their own males, where best is defined by the weakest response to the signal and the highest fitness. We test these hypotheses by crossing strains generated from a formal model of sexually antagonistic coevolution. Strains differ in the strength of natural selection acting on male and female traits. In our model, we assume sexually antagonistic coevolution of a single male signal and female receptor. The female receptor is treated as a preference function where both the slope and intercept of the function can evolve. Our results suggest that neither prediction is consistently supported. Interactions are not diagnostic of complex signal-receiver systems, and even under sexually antagonistic coevolution, females may do better mating with males of strains other than their own. These results suggest a reinterpretation of several recent experiments and have important implications for developing theories of speciation when sexually antagonistic coevolution is involved.

Full Text

The Full Text of this article is available as a PDF (216.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aguadé M. Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. Genetics. 1999 Jun;152(2):543–551. doi: 10.1093/genetics/152.2.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andrés J. A., Arnqvist G. Genetic divergence of the seminal signal-receptor system in houseflies: the footprints of sexually antagonistic coevolution? Proc Biol Sci. 2001 Feb 22;268(1465):399–405. doi: 10.1098/rspb.2000.1392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Arak A., Enquist M. Conflict, receiver bias and the evolution of signal form. Philos Trans R Soc Lond B Biol Sci. 1995 Sep 29;349(1330):337–344. doi: 10.1098/rstb.1995.0122. [DOI] [PubMed] [Google Scholar]
  4. Arnqvist G, Nilsson T. The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav. 2000 Aug;60(2):145–164. doi: 10.1006/anbe.2000.1446. [DOI] [PubMed] [Google Scholar]
  5. Arnqvist Göran, Rowe Locke. Antagonistic coevolution between the sexes in a group of insects. Nature. 2002 Feb 14;415(6873):787–789. doi: 10.1038/415787a. [DOI] [PubMed] [Google Scholar]
  6. Arnqvist Göran, Rowe Locke. Correlated evolution of male and female morphologles in water striders. Evolution. 2002 May;56(5):936–947. doi: 10.1111/j.0014-3820.2002.tb01406.x. [DOI] [PubMed] [Google Scholar]
  7. Basolo A. L. Evolutionary change in a receiver bias: a comparison of female preference functions. Proc Biol Sci. 1998 Nov 22;265(1411):2223–2228. doi: 10.1098/rspb.1998.0563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brown D. V., Eady P. E. Functional incompatibility between the fertilization systems of two allopatric populations of Callosobruchus maculatus (Coleoptera: Bruchidae). Evolution. 2001 Nov 11;55(11):2257–2262. doi: 10.1111/j.0014-3820.2001.tb00740.x. [DOI] [PubMed] [Google Scholar]
  9. Chapman T., Liddle L. F., Kalb J. M., Wolfner M. F., Partridge L. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature. 1995 Jan 19;373(6511):241–244. doi: 10.1038/373241a0. [DOI] [PubMed] [Google Scholar]
  10. Chapman T. Seminal fluid-mediated fitness traits in Drosophila. Heredity (Edinb) 2001 Nov;87(Pt 5):511–521. doi: 10.1046/j.1365-2540.2001.00961.x. [DOI] [PubMed] [Google Scholar]
  11. Civetta A., Singh R. S. High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J Mol Evol. 1995 Dec;41(6):1085–1095. doi: 10.1007/BF00173190. [DOI] [PubMed] [Google Scholar]
  12. Clark A. G., Begun D. J., Prout T. Female x male interactions in Drosophila sperm competition. Science. 1999 Jan 8;283(5399):217–220. doi: 10.1126/science.283.5399.217. [DOI] [PubMed] [Google Scholar]
  13. Gavrilets S., Arnqvist G., Friberg U. The evolution of female mate choice by sexual conflict. Proc Biol Sci. 2001 Mar 7;268(1466):531–539. doi: 10.1098/rspb.2000.1382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gavrilets S. Rapid evolution of reproductive barriers driven by sexual conflict. Nature. 2000 Feb 24;403(6772):886–889. doi: 10.1038/35002564. [DOI] [PubMed] [Google Scholar]
  15. Holland B., Rice W. R. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5083–5088. doi: 10.1073/pnas.96.9.5083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hosken D. J., Blanckenhorn W. U., Garner T. W. J. Heteropopulation males have a fertilization advantage during sperm competition in the yellow dung fly (Scathophaga stercoraria). Proc Biol Sci. 2002 Aug 22;269(1501):1701–1707. doi: 10.1098/rspb.2002.2094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hosken D. J., Garner T. W., Ward P. I. Sexual conflict selects for male and female reproductive characters. Curr Biol. 2001 Apr 3;11(7):489–493. doi: 10.1016/s0960-9822(01)00146-4. [DOI] [PubMed] [Google Scholar]
  18. Houde A. E., Endler J. A. Correlated Evolution of Female Mating Preferences and Male Color Patterns in the Guppy Poecilia reticulata. Science. 1990 Jun 15;248(4961):1405–1408. doi: 10.1126/science.248.4961.1405. [DOI] [PubMed] [Google Scholar]
  19. Knowles L. L., Markow T. A. Sexually antagonistic coevolution of a postmating-prezygotic reproductive character in desert Drosophila. Proc Natl Acad Sci U S A. 2001 Jul 10;98(15):8692–8696. doi: 10.1073/pnas.151123998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lande R. Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3721–3725. doi: 10.1073/pnas.78.6.3721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Miller G. T., Pitnick S. Functional significance of seminal receptacle length in Drosophila melanogaster. J Evol Biol. 2003 Jan;16(1):114–126. doi: 10.1046/j.1420-9101.2003.00476.x. [DOI] [PubMed] [Google Scholar]
  22. Miller Gary T., Pitnick Scott. Sperm-female coevolution in Drosophila. Science. 2002 Nov 8;298(5596):1230–1233. doi: 10.1126/science.1076968. [DOI] [PubMed] [Google Scholar]
  23. Nilsson Tina, Fricke Claudia, Arnqvist Goran. Patterns of divergence in the effects of mating on female reproductive performance in flour beetles. Evolution. 2002 Jan;56(1):111–120. doi: 10.1111/j.0014-3820.2002.tb00853.x. [DOI] [PubMed] [Google Scholar]
  24. doi: 10.1098/rspb.1999.0741. [DOI] [PMC free article] [Google Scholar]
  25. Palumbi S. R., Metz E. C. Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). Mol Biol Evol. 1991 Mar;8(2):227–239. doi: 10.1093/oxfordjournals.molbev.a040642. [DOI] [PubMed] [Google Scholar]
  26. Panhuis T. M., Butlin R., Zuk M., Tregenza T. Sexual selection and speciation. Trends Ecol Evol. 2001 Jul 1;16(7):364–371. doi: 10.1016/s0169-5347(01)02160-7. [DOI] [PubMed] [Google Scholar]
  27. Parker G. A., Partridge L. Sexual conflict and speciation. Philos Trans R Soc Lond B Biol Sci. 1998 Feb 28;353(1366):261–274. doi: 10.1098/rstb.1998.0208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pitnick S., Brown W. D., Miller G. T. Evolution of female remating behaviour following experimental removal of sexual selection. Proc Biol Sci. 2001 Mar 22;268(1467):557–563. doi: 10.1098/rspb.2000.1400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Pitnick S., Miller G. T., Reagan J., Holland B. Males' evolutionary responses to experimental removal of sexual selection. Proc Biol Sci. 2001 May 22;268(1471):1071–1080. doi: 10.1098/rspb.2001.1621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rice W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature. 1996 May 16;381(6579):232–234. doi: 10.1038/381232a0. [DOI] [PubMed] [Google Scholar]
  31. Rowe Locke, Arnqvist Göran. Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to address evolutionary processes. Evolution. 2002 Apr;56(4):754–767. doi: 10.1111/j.0014-3820.2002.tb01386.x. [DOI] [PubMed] [Google Scholar]
  32. 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 U S A. 2001 Feb 20;98(5):2509–2514. doi: 10.1073/pnas.051605998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Swanson Willie J., Vacquier Victor D. The rapid evolution of reproductive proteins. Nat Rev Genet. 2002 Feb;3(2):137–144. doi: 10.1038/nrg733. [DOI] [PubMed] [Google Scholar]
  34. Wagner WE. Measuring female mating preferences. Anim Behav. 1998 Apr;55(4):1029–1042. doi: 10.1006/anbe.1997.0635. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES