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 Mar 22;270(1515):653–664. doi: 10.1098/rspb.2002.2235

The evolution of mate choice and mating biases.

Hanna Kokko 1, Robert Brooks 1, Michael D Jennions 1, Josephine Morley 1
PMCID: PMC1691281  PMID: 12769467

Abstract

We review the current status of three well-established models (direct benefits, indirect benefits and sensory drive) and one newcomer (antagonistic chase-away) of the evolution of mate choice and the biases that are expressed during choice. We highlight the differences and commonalities in the underlying genetics and evolutionary dynamics of these models. We then argue that progress in understanding the evolution of mate choice is currently hampered by spurious distinctions among models and a misguided tendency to test the processes underlying each model as mutually exclusive alternatives. Finally, we suggest potentially fruitful directions for future theoretical and empirical research.

Full Text

The Full Text of this article is available as a PDF (287.4 KB).

Selected References

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

  1. Agrawal A. F. Sexual selection and the maintenance of sexual reproduction. Nature. 2001 Jun 7;411(6838):692–695. doi: 10.1038/35079590. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. 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]
  4. Barton N. H., Turelli M. Evolutionary quantitative genetics: how little do we know? Annu Rev Genet. 1989;23:337–370. doi: 10.1146/annurev.ge.23.120189.002005. [DOI] [PubMed] [Google Scholar]
  5. Blows M. W. Evolution of the genetic covariance between male and female components of mate recognition: an experimental test. Proc Biol Sci. 1999 Nov 7;266(1434):2169–2174. doi: 10.1098/rspb.1999.0904. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Blows Mark W. Interaction between natural and sexual selection during the evolution of mate recognition. Proc Biol Sci. 2002 Jun 7;269(1496):1113–1118. doi: 10.1098/rspb.2002.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Boake C. R. Genetic consequences of mate choice: a quantitative genetic method for testing sexual selection theory. Science. 1985 Mar 1;227(4690):1061–1063. doi: 10.1126/science.227.4690.1061. [DOI] [PubMed] [Google Scholar]
  8. Brooks R., Endler J. A. Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution. 2001 May;55(5):1002–1015. doi: 10.1554/0014-3820(2001)055[1002:daissa]2.0.co;2. [DOI] [PubMed] [Google Scholar]
  9. Brooks R., Kemp D. J. Can older males deliver the good genes? Trends Ecol Evol. 2001 Jun 1;16(6):308–313. doi: 10.1016/s0169-5347(01)02147-4. [DOI] [PubMed] [Google Scholar]
  10. Brooks R. Negative genetic correlation between male sexual attractiveness and survival. Nature. 2000 Jul 6;406(6791):67–70. doi: 10.1038/35017552. [DOI] [PubMed] [Google Scholar]
  11. Bulmer M. Structural instability of models of sexual selection. Theor Popul Biol. 1989 Apr;35(2):195–206. doi: 10.1016/0040-5809(89)90017-8. [DOI] [PubMed] [Google Scholar]
  12. Candolin U. Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks. Proc Biol Sci. 2000 Dec 7;267(1460):2425–2430. doi: 10.1098/rspb.2000.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. 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]
  14. Chippindale A. K., Gibson J. R., Rice W. R. Negative genetic correlation for adult fitness between sexes reveals ontogenetic conflict in Drosophila. Proc Natl Acad Sci U S A. 2001 Jan 30;98(4):1671–1675. doi: 10.1073/pnas.041378098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Cordero C., Eberhard W. G. Female choice of sexually antagonistic male adaptations: a critical review of some current research. J Evol Biol. 2003 Jan;16(1):1–6. doi: 10.1046/j.1420-9101.2003.00506.x. [DOI] [PubMed] [Google Scholar]
  16. Crudgington H. S., Siva-Jothy M. T. Genital damage, kicking and early death. Nature. 2000 Oct 19;407(6806):855–856. doi: 10.1038/35038154. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Gilburn AS, Day TH. Female mating behaviour, sexual selection and chromosome I inversion karyotype in the seaweed fly, coelopa frigida . Heredity (Edinb) 1999 Apr;82(Pt 3):276–281. doi: 10.1038/sj.hdy.6884830. [DOI] [PubMed] [Google Scholar]
  19. Grafen A. Biological signals as handicaps. J Theor Biol. 1990 Jun 21;144(4):517–546. doi: 10.1016/s0022-5193(05)80088-8. [DOI] [PubMed] [Google Scholar]
  20. Hall D. W., Kirkpatrick M., West B. Runaway sexual selection when female preferences are directly selected. Evolution. 2000 Dec;54(6):1862–1869. doi: 10.1554/0014-3820(2000)054[1862:RSSWFP]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  21. Hamilton W. D., Zuk M. Heritable true fitness and bright birds: a role for parasites? Science. 1982 Oct 22;218(4570):384–387. doi: 10.1126/science.7123238. [DOI] [PubMed] [Google Scholar]
  22. Hine Emma, Lachish Shelly, Higgie Megan, Blows Mark W. Positive genetic correlation between female preference and offspring fitness. Proc Biol Sci. 2002 Nov 7;269(1506):2215–2219. doi: 10.1098/rspb.2002.2149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. 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]
  24. Houle David, Kondrashov Alexey S. Coevolution of costly mate choice and condition-dependent display of good genes. Proc Biol Sci. 2002 Jan 7;269(1486):97–104. doi: 10.1098/rspb.2001.1823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Iwasa Y., Pomiankowski A. Continual change in mate preferences. Nature. 1995 Oct 5;377(6548):420–422. doi: 10.1038/377420a0. [DOI] [PubMed] [Google Scholar]
  26. Iwasa Y., Pomiankowski A. Good parent and good genes models of handicap evolution. J Theor Biol. 1999 Sep 7;200(1):97–109. doi: 10.1006/jtbi.1999.0979. [DOI] [PubMed] [Google Scholar]
  27. Iyengar V. K., Eisner T. Heritability of body mass, a sexually selected trait, in an arctiid moth (Utetheisa ornatrix). Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9169–9171. doi: 10.1073/pnas.96.16.9169. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Iyengar Vikram K., Reeve H. Kern, Eisner Thomas. Paternal inheritance of a female moth's mating preference. Nature. 2002 Oct 24;419(6909):830–832. doi: 10.1038/nature01027. [DOI] [PubMed] [Google Scholar]
  29. Jennions M. D., Møller A. P., Petrie M. Sexually selected traits and adult survival: a meta-analysis. Q Rev Biol. 2001 Mar;76(1):3–36. doi: 10.1086/393743. [DOI] [PubMed] [Google Scholar]
  30. Kirkpatrick M., Barton N. H. The strength of indirect selection on female mating preferences. Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1282–1286. doi: 10.1073/pnas.94.4.1282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kokko Hanna, Brooks Robert, McNamara John M., Houston Alasdair I. The sexual selection continuum. Proc Biol Sci. 2002 Jul 7;269(1498):1331–1340. doi: 10.1098/rspb.2002.2020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kotiaho J. S., Simmons L. W., Tomkins J. L. Towards a resolution of the lek paradox. Nature. 2001 Apr 5;410(6829):684–686. doi: 10.1038/35070557. [DOI] [PubMed] [Google Scholar]
  33. Kruuk L. E., Clutton-Brock T. H., Slate J., Pemberton J. M., Brotherstone S., Guinness F. E. Heritability of fitness in a wild mammal population. Proc Natl Acad Sci U S A. 2000 Jan 18;97(2):698–703. doi: 10.1073/pnas.97.2.698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Merilä J, Sheldon BC. Lifetime Reproductive Success and Heritability in Nature. Am Nat. 2000 Mar;155(3):301–310. doi: 10.1086/303330. [DOI] [PubMed] [Google Scholar]
  36. Moore Sarah L., Wilson Kenneth. Parasites as a viability cost of sexual selection in natural populations of mammals. Science. 2002 Sep 20;297(5589):2015–2018. doi: 10.1126/science.1074196. [DOI] [PubMed] [Google Scholar]
  37. Møller A. P., Jennions M. D. How important are direct fitness benefits of sexual selection? Naturwissenschaften. 2001 Oct;88(10):401–415. doi: 10.1007/s001140100255. [DOI] [PubMed] [Google Scholar]
  38. doi: 10.1098/rspb.1997.0042. [DOI] [PMC free article] [Google Scholar]
  39. doi: 10.1098/rspb.1998.0484. [DOI] [PMC free article] [Google Scholar]
  40. doi: 10.1098/rspb.1998.0515. [DOI] [PMC free article] [Google Scholar]
  41. doi: 10.1098/rspb.1999.0832. [DOI] [PMC free article] [Google Scholar]
  42. Pitnick Scott, García-González Francisco. Harm to females increases with male body size in Drosophila melanogaster. Proc Biol Sci. 2002 Sep 7;269(1502):1821–1828. doi: 10.1098/rspb.2002.2090. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Qvarnström A., Pärt T., Sheldon B. C. Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature. 2000 May 18;405(6784):344–347. doi: 10.1038/35012605. [DOI] [PubMed] [Google Scholar]
  44. Rhen T. Sex-limited mutations and the evolution of sexual dimorphism. Evolution. 2000 Feb;54(1):37–43. doi: 10.1111/j.0014-3820.2000.tb00005.x. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. 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]
  47. Rodd F. Helen, Hughes Kimberly A., Grether Gregory F., Baril Colette T. A possible non-sexual origin of mate preference: are male guppies mimicking fruit? Proc Biol Sci. 2002 Mar 7;269(1490):475–481. doi: 10.1098/rspb.2001.1891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Semple S. The function of Barbary macaque copulation calls. Proc Biol Sci. 1998 Feb 22;265(1393):287–291. doi: 10.1098/rspb.1998.0294. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Siller S., Department of Zoology, University of Oxford, UK. steven.siller@zoo.ox.ac.uk Sexual selection and the maintenance of sex. Nature. 2001 Jun 7;411(6838):689–692. doi: 10.1038/35079578. [DOI] [PubMed] [Google Scholar]
  50. Welch A. M., Semlitsch R. D., Gerhardt H. C. Call duration as an indicator of genetic quality in male gray tree frogs. Science. 1998 Jun 19;280(5371):1928–1930. doi: 10.1126/science.280.5371.1928. [DOI] [PubMed] [Google Scholar]
  51. Whitlock M. C. Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution. 2000 Dec;54(6):1855–1861. doi: 10.1111/j.0014-3820.2000.tb01232.x. [DOI] [PubMed] [Google Scholar]
  52. Zahavi A. Mate selection-a selection for a handicap. J Theor Biol. 1975 Sep;53(1):205–214. doi: 10.1016/0022-5193(75)90111-3. [DOI] [PubMed] [Google Scholar]

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

RESOURCES