Genetica

, Volume 116, Issue 2–3, pp 343–358

Variation in Female Mate Choice within Guppy Populations: Population Divergence, Multiple Ornaments and the Maintenance of Polymorphism

  • Robert Brooks
Article

Abstract

The evolutionary significance of variation in mate choice behaviour is currently a subject of some debate and considerable empirical study. Here, I review recent work on variation within and among guppy (Poecilia reticulata) populations in female mate choice and mating preferences. Empirical results demonstrate that there is substantial variation within and among populations in female responsiveness and choosiness, and much of this variation is genetic. Evidence for variation in preference functions also exists, but this appears to be more equivocal and the relative importance of genetic variation is less clear cut. In the second half of this review I discuss the potential significance of this variation to three important evolutionary issues: the presence of multiple male ornaments, the maintenance of polymorphism and divergence in mate recognition among populations. Studies of genetic variation in mate choice within populations indicate that females have complex, multivariate preferences that are able to evolve independently to some extent. These findings suggest that the presence of multiple male ornaments may be due to multiple female mating preferences. The extreme polymorphism in male guppy colour patterns demands explanation, yet no single satisfactory explanation has yet emerged. I review several old ideas and a few new ones in order to identify the most promising potential explanations for future empirical testing. Among these are negative frequency dependent selection, environmental heterogeneity coupled with gene flow, and genetic constraints. Last, I review the relative extent of within and among-population variation in mate choice and mating preferences in order to assess why guppies have not speciated despite a history of isolation and divergence. I argue that variation within guppy populations in mate choice and enhanced mating success of new immigrants to a pool are major impediments to population divergence of the magnitude that would be required for speciation to occur.

frequency dependence guppy heritability mate choice polymorphism preference repeatability speciation variation 

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References

  1. Andersson, M., 1994. Sexual Selection. Princeton University Press, Princeton, NJ.Google Scholar
  2. Badyaev, A.V., G.E. Hill, P.O. Dunn & J.C. Glen, 2001. Plumage color as a composite trait: developmental and functional integration of sexual ornamentation. Am. Nat. 158: 221–235.Google Scholar
  3. Baerends, G.P., R. Brouwer & H.T.J. Waterbolk, 1955. Ethological studies on Lebistes reticulatus (Peters). 1. An analysis of the male courtship pattern. Behaviour 8: 249–334.Google Scholar
  4. Bakker, T.C.M. & A. Pomiankowski, 1995. The genetic basis of female mate preferences. J. Evol. Biol. 8: 129–171.Google Scholar
  5. Barton, N.H. & M. Turelli, 1989. Evolutionary quantitative genetics: how little do we know. Annu. Rev. Genet. 23: 337–370.Google Scholar
  6. Becher, S.A. & A.E. Magurran, 2000. Gene flow in Trinidadian guppies. J. Fish Biol. 56: 241–249.Google Scholar
  7. Boake, C.R.B., 1989. Repeatability: its role in evolutionary studies of mating behaviour. Evol. Ecol. 3: 173–182.Google Scholar
  8. Bond, A.B. & A.C. Kamil, 1998. Apostatic selection by blue jays produces balanced polymorphism in virtual prey. Nature 395: 594–596.Google Scholar
  9. Boughman, J.W., 2001. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411: 944–947.Google Scholar
  10. Breden, F. & K. Hornaday, 1994. Test of indirect models of selection in the Trinidad guppy. Heredity 73: 291–297.Google Scholar
  11. Brooks, R., 1996. Copying and the repeatability of mate choice. Behav. Ecol. Sociobiol. 39: 323–329.Google Scholar
  12. Brooks, R., 2000. Negative genetic correlation between male sexual attractiveness and survival. Nature 406: 67–70.Google Scholar
  13. Brooks, R. & N. Caithness, 1995. Female choice in a feral guppy population: are there multiple cues? Anim. Behav. 50: 301–307.Google Scholar
  14. Brooks, R. & V. Couldridge, 1999. Multiple sexual ornaments coevolve with multiple mating preferences. Am. Nat. 154: 37–45.Google Scholar
  15. Brooks, R. & J.A. Endler, 2001a. Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55: 1002–1015.Google Scholar
  16. Brooks, R. & J.A. Endler, 2001b. Female guppies agree to differ: phenotypic and genetic variation in mate-choice behaviour and the consequences for sexual selection. Evolution 55: 1644–1655.Google Scholar
  17. Crow, R.T. & N.R. Liley, 1979. A sexual pheromone in the guppy, Poecilia reticulata (Peters). Can. J. Zoo. 57: 184–188.Google Scholar
  18. Endler, J.A., 1978. A predator's view of animal colour patterns. Evol. Biol. 11: 319–364.Google Scholar
  19. Endler, J.A., 1980. Natural selection on color patterns in Poecilia reticulata. Evolution 34: 76–91.Google Scholar
  20. Endler, J.A., 1983. Natural and sexual selection on color patterns in poeciliid fishes. Environ. Biol. Fishes 9: 173–190.Google Scholar
  21. Endler, J.A., 1987. Predation, light intensity and courtship behaviour in Poecilia reticulata (Pisces: Poeciliidae). Anim. Behav. 35: 1376–1385.Google Scholar
  22. Endler, J.A., 1991. Variation in the appearance of guppy color patterns to guppies and their predators under different visual conditions. Vision Res. 31: 587–608.Google Scholar
  23. Endler, J.A., 1992. Signals, signal conditions, and the direction of evolution. Am. Nat. 139: S125–S153.Google Scholar
  24. Endler, J.A., 1993. Some general comments on the evolution and design of animal communication systems. Philos. Trans. R. Soc. Lond. Ser. B 340: 215–225.Google Scholar
  25. Endler, J.A., 1995. Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol. Evol. 10: 22–29.Google Scholar
  26. Endler, J.A. & A. Basolo, 1998. Sensory ecology, receiver biases and sexual selection. Trends Ecol. Evol. 13: 415–420.Google Scholar
  27. Endler, J.A. & A.E. Houde, 1995. Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution 49: 456–468.Google Scholar
  28. Endler, J.A., D. Westcott, J. Madden & T. Robson, unpub. ms. Innovation and signal efficiency affect the outcome of sexual selection in bowerbirds but elaboration does not.Google Scholar
  29. Evans, J.P. & A.E. Magurran, 2000. Multiple benefits of multiple mating in guppies. Proc. Natl. Acad. Sci. USA 97: 10074–10076.Google Scholar
  30. Fajen, A. & F. Breden, 1992. Mitochondrial DNA sequence variation among natural populations of the Trinidad guppy, Poecilia reticulata. Evolution 46: 1457–1465.Google Scholar
  31. Falconer, D.S. & T.F.C. Mackay, 1996. Introduction to Quantitative Genetics. Longman, New York, 4th edn.Google Scholar
  32. Farr, J.A., 1977. Male rarity or novelty, female choice behaviour, and sexual selection in the guppy, Poecilia reticulata Peters (Pisces: Poeciliidae). Evolution 31: 162–168.Google Scholar
  33. Farr, J.A., 1980. Social behavior patterns as determinants of reproductive success in the guppy, Poecilia reticulata Peters (Pisces: Poeciliidae). An experimental study of the effects of intermale competition, female choice, and sexual selection. Behaviour 74: 38–91.Google Scholar
  34. Farr, J.A. & K. Peters, 1984. The inheritance of quantitative fitness traits in guppies, Poecilia reticulata (Pisces: Poeciliidae): tests for inbreeding effects. Heredity 52: 285–296.Google Scholar
  35. Fisher, R.A., 1930. The Genetical Theory of Natural Selection. Oxford University Press, Oxford.Google Scholar
  36. Gamble, S.L., 2001. The Effect of Ambient Light Spectra in Male Mating Strategies and Female Response in the Guppy. The University of New South Wales, Sydney.Google Scholar
  37. Glanville, P.W. & J.A. Allen, 1997. Protective polymorphism in populations of computer-simulated moth-like prey. Oikos 80: 565–571.Google Scholar
  38. Godin, J.J. & L.A. Dugatkin, 1995. Variability and repeatability of female mating preference in the guppy. Anim. Behav. 49: 1427–1433.Google Scholar
  39. Gray, D.A. & W.H. Cade, 2000. Sexual selection and speciation in field crickets. Proc. Natl. Acad. Sci. USA 97: 14449–14454.Google Scholar
  40. Gray, D.A. & W.H. Cade, 1999. Correlated-response-to-selection experiments designed to test for a genetic correlation between female preferences and male traits yeild biased results. Anim. Behav. 58: 1325–1327.Google Scholar
  41. Grether, G.F., J. Hudon & D.F. Millie, 1999. Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc. R. Soc. Lond. Ser. B 266: 1317–1322.Google Scholar
  42. Guilford, T. & M. Stamp Dawkins, 1991. Receiver psychology and the evolution of animal signals. Anim. Behav. 42: 1–14.Google Scholar
  43. Haskins, C.P. & E.F. Haskins, 1961. Polymorphism and population structure in Lebistes reticulatus. pp. 320–395 in Vertebrate Speciation, edited by W.F. Blair. University of Texas Press, Austin.Google Scholar
  44. Hoffmann, A.A., 1999. Is the heritability for courtship and mating speed in Drosophila (fruit fly) low? Heredity 82: 158–162.Google Scholar
  45. Houde, A.E., 1992. Sex-linked heritability of a sexually selected character in a natural population of Poecilia reticulata (Pisces: Poeciliidae) (guppies). Heredity 69: 229–235.Google Scholar
  46. Houde, A.E., 1994. Effect of artificial selection on male colour patterns on mating preference of female guppies. Proc. R. Soc. Lond. Ser. B 256: 125–130.Google Scholar
  47. Houde, A.E., 1997. Sex, Color and Mate Choice in Guppies.Princeton University Press, Princeton, NJ.Google Scholar
  48. Houde, A.E. & J.A. Endler, 1990. Correlated evolution of female mating preferences and male color patterns in the guppy Poecilia reticulata. Science 248: 1405–1408.Google Scholar
  49. Hughes, K.A., L. Du, F.H. Rodd & D.N. Reznick, 1999. Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Anim. Behav. 58: 907–916.Google Scholar
  50. Jennions, M.D. & M. Petrie, 1997. Variation in mate choice and mating preferences: a review of causes and consequences. Biol. Rev. Camb. Phil. Soc. 72: 283–327.Google Scholar
  51. Johnstone, R.A., 1995. Honest advertisement of multiple qualities using multiple signals. J. Theor. Biol. 177: 87–94.Google Scholar
  52. Johnstone, R.A., 1996. Multiple displays in animal communication: ‘backup signals’ and ‘multiple messages’. Philos. Trans. R. Soc. Lond. Ser. B 351: 329–338.Google Scholar
  53. Karino, K. & Y. Haijima, 2001. Heritability of male secondary sexual traits in feral guppies in Japan. J. Ethol. 19: 33–37.Google Scholar
  54. Kelley, J.L., J.A. Graves & A.E. Magurran, 1999. Familiarity breeds contempt in guppies. Nature 401: 661.Google Scholar
  55. Kelly, C.D., J.-G.J. Godin & J.M. Wright, 1999. Geographical variation in multiple paternity within natural populations of the guppy (Poecilia reticulata). Proc. R. Soc. Lond. Ser. B 266: 2403–2408.Google Scholar
  56. Kirkpatrick, M. & M.J. Ryan, 1991. The evolution of mating preferences and the paradox of the lek. Nature 350: 33–38.Google Scholar
  57. Kodric-Brown, A. & P.F. Nicoletto, 1997. Repeatability of female choice in the guppy: response to live and videotaped males. Anim. Behav. 54: 369–376.Google Scholar
  58. Kotiaho, J.S., L.W. Simmons & J.L. Tomkins, 2001. Towards a resolution of the lek paradox. Nature 410: 684–686.Google Scholar
  59. Lande, R., 1981. Models of speciation by sexual selection on polygenic traits. Proc. Natl. Acad. Sci. USA 78: 3721–3725.Google Scholar
  60. Liley, N.R., 1966. Ethological isolating mechanisms in four sympatric species of poeciliid fishes. Behaviour 13(suppl.): 1–197.Google Scholar
  61. Magurran, A.E., 1998. Population differentiation without speciation. Phil. Trans. R. Soc. Lond. Ser. B 353: 275–286.Google Scholar
  62. Matthews, I.M. & A.E. Magurran, 2000. Evidence for sperm transfer during sneaky mating in wild Trinidadian guppies. J. Fish Biol. 56: 1381–1386.Google Scholar
  63. Maynard Smith, J., 1998. Evolutionary Genetics. Oxford University Press, Oxford.Google Scholar
  64. Møller, A.P. & A. Pomiankowski, 1993. Why have birds got multiple sexual ornaments? Behav. Ecol. Sociobiol. 32: 167–176.Google Scholar
  65. Moore, A.J. & P.J. Moore, 1999. Balancing sexual selection through opposing mate choice and male competition. Proc. Roy. Soc. Lond. Ser. B 266: 711–716.Google Scholar
  66. Panhuis, T.M., R.K. Butlin, M. Zuk & T. Tregenza, 2001. Sexual selection and speciation. Trends Ecol. Evol. 16: 325–413.Google Scholar
  67. Partridge, L., 1988. The rare-male effect; what is its evolutionary significance? Phil. Trans. R. Soc. Lond. Ser. B 319: 525–539.Google Scholar
  68. Partridge, L., 1989. Frequency-dependent mating preferences in female fruitflies? Behav. Genet. 19: 725–728.Google Scholar
  69. Partridge, L. & W.G. Hill, 1984. Mechanisms for frequencydependent mating success. Biol. J. Linnean Soc. 23: 113–132.Google Scholar
  70. Pomiankowski, A. & Y. Iwasa, 1993. Evolution of multiple sexual preferences by Fisher's runaway process of sexual selection. Proc. R. Soc. Lond. Ser B 253: 173–181.Google Scholar
  71. Pomiankowski, A. & Y. Iwasa, 1998. Runaway ornament diversity caused by Fisherian sexual selection. Proc. Natl. Acad. Sci. USA 95: 5106–5111.Google Scholar
  72. Pomiankowski, A. & A.P. Møller, 1995. A resolution of the lek paradox. Proc. R. Soc. Lond. Ser. B 260: 21–29.Google Scholar
  73. Pomiankowski, A. & L. Sheridan, 1994. Linked sexiness and choosiness. Trends Ecol. Evol. 9: 242–244.Google Scholar
  74. Ptacek, M.B., 2000. The role of mating preferences in sapping interspecific divergence in mating signals in vertebrates. Behav. Process. 51: 111–134.Google Scholar
  75. Rodd, F.H., K.A. Hughes, G.F. Grether & C.T. Baril, 2001. A possible non-sexual origin of a mate preference: are male guppies mimicking fruit? Proc. R. Soc. Lond. Ser. B 269: 475–481.Google Scholar
  76. Rowe, C., 1999. Reciever psychology and the evolution of multicomponent signals. Anim. Behav. 58: 921–931.Google Scholar
  77. Rowe, L. & D. Houle, 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. R. Soc. Lond. Ser. B 263: 1415–1421.Google Scholar
  78. Ryan, M.J. & A.S. Rand, 1993. Species recognition and sexual selection as a unitary problem in animal communication. Evolution 47: 647–657.Google Scholar
  79. Schluter, D., 2001. Ecology and the origin of species. Trends Ecol. Evol. 16: 325–413.Google Scholar
  80. Shaw, P.W., G.R. Carvalho, B.H. Seghers & A.E. Magurran, 1992. Genetic consequences of an artificial introduction of guppies (Poecilia reticulata) in N. Trinidad. Proc. R. Soc. Lond. Ser. B 248: 111–116.Google Scholar
  81. Spiess, E.B. & L. Ehrman, 1978. Rare male mating advantage. Nature 272: 188–189.Google Scholar
  82. Taylor, P.D.& G.C. Williams, 1982. The lek paradox is not resolved. Theor. Popul. Biol. 22: 392–409.Google Scholar
  83. Widemo, F. & S.A. Sæther, 1999. Beauty is in the eye of the beholder: causes and consequences of variation in mating preferences. Trends Ecol. Evol. 14: 26–31.Google Scholar
  84. Winge, Ö., 1922. A peculiar mode of inheritance and its cytological explanation. J. Genet. 12: 137–144.Google Scholar
  85. Winge, Ö., 1927. The location of eighteen genes in Lebistes reticulatus. J. Genet. 18: 1–42.Google Scholar
  86. Winge, Ö. & E. Ditlevsen, 1947. Colour inheritance and sex determination in Lebistes. Heredity 1: 65–83.Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • Robert Brooks
    • 1
  1. 1.School of Biological, Earth and Environmental SciencesThe University of New South WalesSydneyAustralia (Phone

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