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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1998 Feb 28;353(1366):261–274. doi: 10.1098/rstb.1998.0208

Sexual conflict and speciation.

G A Parker 1, L Partridge 1
PMCID: PMC1692203  PMID: 9533125

Abstract

We review the significance of two forms of sexual conflict (different evolutionary interests of the two sexes) for genetic differentiation of populations and the evolution of reproductive isolation. Conflicting selection on the alleles at a single locus can occur in males and females if the sexes have different optima for a trait, and there are pleiotropic genetic correlations between the sexes for it. There will then be selection for sex limitation and hence sexual dimorphism. This sex limitation could break down in hybrids and reduce their fitness. Pleiotropic genetic correlations between the sexes could also affect the likelihood of mating in interpopulation encounters. Conflict can also occur between (sex-limited) loci that determine behaviour in males and those that determine behaviour in females. Reproductive isolation may occur by rapid coevolution of male trait and female mating preference. This would tend to generate assortative mating on secondary contact, hence promoting speciation. Sexual conflict resulting from sensory exploitation, polyspermy and the cost of mating could result in high levels of interpopulation mating. If females evolve resistance to make pre- and postmating manipulation, males from one population could be more successful with females from the other, because females would have evolved resistance to their own (but not to the allopatric) males. Between-locus sexual conflict could also occur as a result of conflict between males and females of different populations over the production of unfit hybrids. We develop models which show that females are in general selected to resist such matings and males to persist, and this could have a bearing on both the initial level of interpopulation matings and the likelihood that reinforcement will occur. In effect, selection on males usually acts to promote gene flow and to restrict premating isolation, whereas selection on females usually acts in the reverse direction. We review theoretical models relevant to resolution of this conflict. The winning role depends on a balance between the 'value of winning' and 'power' (relating to contest or armament costs): the winning role is likely to correlate with high value of winning and low costs. Sperm-ovum (or sperm-female tract) conflicts (and their plant parallels) are likely to obey the same principles. Males may typically have higher values of winning, but it is difficult to quantify 'power', and females may often be able to resist mating more cheaply than males can force it. We tentatively predict that sexual conflict will typically result in a higher rate of speciation in 'female-win' clades, that females will be responsible for premating isolation through reinforcement, and that 'female-win' populations will be less genetically diverse.

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Selected References

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

  1. Aguadé M., Miyashita N., Langley C. H. Polymorphism and divergence in the Mst26A male accessory gland gene region in Drosophila. Genetics. 1992 Nov;132(3):755–770. doi: 10.1093/genetics/132.3.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BAKER H. G. Reproductive methods as factors in speciation in flowering plants. Cold Spring Harb Symp Quant Biol. 1959;24:177–191. doi: 10.1101/sqb.1959.024.01.019. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Chapman T., Partridge L. Sexual conflict as fuel for evolution. Nature. 1996 May 16;381(6579):189–190. doi: 10.1038/381189a0. [DOI] [PubMed] [Google Scholar]
  5. Chen P. S., Stumm-Zollinger E., Aigaki T., Balmer J., Bienz M., Böhlen P. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell. 1988 Jul 29;54(3):291–298. doi: 10.1016/0092-8674(88)90192-4. [DOI] [PubMed] [Google Scholar]
  6. Clutton-Brock T. H., Parker G. A. Punishment in animal societies. Nature. 1995 Jan 19;373(6511):209–216. doi: 10.1038/373209a0. [DOI] [PubMed] [Google Scholar]
  7. Dawkins R., Krebs J. R. Arms races between and within species. Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):489–511. doi: 10.1098/rspb.1979.0081. [DOI] [PubMed] [Google Scholar]
  8. Endler J. A. Some general comments on the evolution and design of animal communication systems. Philos Trans R Soc Lond B Biol Sci. 1993 May 29;340(1292):215–225. doi: 10.1098/rstb.1993.0060. [DOI] [PubMed] [Google Scholar]
  9. Gems D., Riddle D. L. Longevity in Caenorhabditis elegans reduced by mating but not gamete production. Nature. 1996 Feb 22;379(6567):723–725. doi: 10.1038/379723a0. [DOI] [PubMed] [Google Scholar]
  10. Gilchrist A. S., Partridge L. Heritability of pre-adult viability differences can explain apparent heritability of sperm displacement ability in Drosophila melanogaster. Proc Biol Sci. 1997 Sep 22;264(1386):1271–1275. doi: 10.1098/rspb.1997.0175. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gow N. A., Perera T. H., Sherwood-Higham J., Gooday G. W., Gregory D. W., Marshall D. Investigation of touch-sensitive responses by hyphae of the human pathogenic fungus Candida albicans. Scanning Microsc. 1994;8(3):705–710. [PubMed] [Google Scholar]
  12. 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]
  13. Kelly J. K., Noor M. A. Speciation by reinforcement: a model derived from studies of Drosophila. Genetics. 1996 Jul;143(3):1485–1497. doi: 10.1093/genetics/143.3.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Krakauer D. C., Johnstone R. A. The evolution of exploitation and honesty in animal communication: a model using artificial neural networks. Philos Trans R Soc Lond B Biol Sci. 1995 May 30;348(1325):355–361. doi: 10.1098/rstb.1995.0073. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Noor M. A. Speciation driven by natural selection in Drosophila. Nature. 1995 Jun 22;375(6533):674–675. doi: 10.1038/375674a0. [DOI] [PubMed] [Google Scholar]
  17. Parker G. A. Assessment strategy and the evolution of fighting behaviour. J Theor Biol. 1974 Sep;47(1):223–243. doi: 10.1016/0022-5193(74)90111-8. [DOI] [PubMed] [Google Scholar]
  18. Parker G. A. Why are there so many tiny sperm? Sperm competition and the maintenance of two sexes. J Theor Biol. 1982 May 21;96(2):281–294. doi: 10.1016/0022-5193(82)90225-9. [DOI] [PubMed] [Google Scholar]
  19. Price C. S. Conspecific sperm precedence in Drosophila. Nature. 1997 Aug 14;388(6643):663–666. doi: 10.1038/41753. [DOI] [PubMed] [Google Scholar]
  20. Rice W. R. Sexually antagonistic genes: experimental evidence. Science. 1992 Jun 5;256(5062):1436–1439. doi: 10.1126/science.1604317. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Schluter D., Price T. Honesty, perception and population divergence in sexually selected traits. Proc Biol Sci. 1993 Jul 22;253(1336):117–122. doi: 10.1098/rspb.1993.0089. [DOI] [PubMed] [Google Scholar]
  23. Tilley S. G., Verrell P. A., Arnold S. J. Correspondence between sexual isolation and allozyme differentiation: a test in the salamander Desmognathus ochrophaeus. Proc Natl Acad Sci U S A. 1990 Apr;87(7):2715–2719. doi: 10.1073/pnas.87.7.2715. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. True J. R., Weir B. S., Laurie C. C. A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. Genetics. 1996 Mar;142(3):819–837. doi: 10.1093/genetics/142.3.819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tsaur S. C., Wu C. I. Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila. Mol Biol Evol. 1997 May;14(5):544–549. doi: 10.1093/oxfordjournals.molbev.a025791. [DOI] [PubMed] [Google Scholar]
  26. van den Berg M. J., Thomas G., Hendriks H., van Delden W. A reexamination of the negative assortative mating phenomenon and its underlying mechanism in Drosophila melanogaster. Behav Genet. 1984 Jan;14(1):45–61. doi: 10.1007/BF01066068. [DOI] [PubMed] [Google Scholar]

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