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Frequency-dependent survival in natural guppy populations

Naturevolume 441pages633636 (2006) | Download Citation



The maintenance of genetic variation in traits under natural selection is a long-standing paradox in evolutionary biology1,2,3. Of the processes capable of maintaining variation, negative frequency-dependent selection (where rare types are favoured by selection) is the most powerful, at least in theory1; however, few experimental studies have confirmed that this process operates in nature. One of the most extreme, unexplained genetic polymorphisms is seen in the colour patterns of male guppies (Poecilia reticulata)4,5. Here we manipulated the frequencies of males with different colour patterns in three natural populations to estimate survival rates, and found that rare phenotypes had a highly significant survival advantage compared to common phenotypes. Evidence from humans6,7 and other species8,9 implicates frequency-dependent survival in the maintenance of molecular, morphological and health-related polymorphisms. As a controlled manipulation in nature, this study provides unequivocal support for frequency-dependent survival—an evolutionary process capable of maintaining extreme polymorphism.

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  1. 1

    Lewontin, R. C. The Genetic Basis of Evolutionary Change (Columbia Univ. Press, New York, 1974)

  2. 2

    Charlesworth, B. & Hughes, K. A. in Evolutionary Genetics from Molecules to Morphology (eds Singh, R. S. & Krimbas, C. B.) 369–391 (Cambridge Univ. Press, Cambridge, 2000)

  3. 3

    Turelli, M. & Barton, N. H. Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and GxE interactions. Genetics 166, 1053–1079 (2004)

  4. 4

    Hughes, K. A., Rodd, F. H. & Reznick, D. N. Genetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata). J. Evol. Biol. 18, 35–45 (2005)

  5. 5

    Brooks, R. & Endler, J. A. Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55, 1002–1015 (2001)

  6. 6

    Trachtenberg, E. et al. Advantage of rare HLA supertype in HIV disease progression. Nature Med. 9, 928–935 (2003)

  7. 7

    Borghans, J. A. M., Beltman, J. B. & De Boer, R. J. MHC polymorphism under host–pathogen coevolution. Immunogenetics 55, 732–739 (2004)

  8. 8

    Reid, D. G. Natural selection for apostasy and crypsis acting on the shell colour polymorphism of a mangrove snail, Littoraria filosa (Sowerby) (Gastropodia: Littoriniidae). Biol. J. Linn. Soc. 30, 1–24 (1987)

  9. 9

    Sinervo, B., Bleay, C. & Adamopoulou, C. Social causes of correlational selection and the resolution of a heritable throat color polymorphism in a lizard. Evolution 55, 2040–2052 (2001)

  10. 10

    Houde, A. E. Sex, Color and Mate Choice in Guppies (Princeton Univ. Press Monographs in Behavioral Ecology, Princeton, 1997)

  11. 11

    Kodric-Brown, A. Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav. Ecol. Sociobiol. 25, 393–401 (1989)

  12. 12

    Grether, G. F. Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata). Evolution 54, 1712–1724 (2000)

  13. 13

    Endler, J. A. & Houde, A. E. Geographic variation in female preferences for male traits in Poecilia reticulata. Evolution 49, 456–468 (1995)

  14. 14

    Endler, J. A. Natural selection on color pattern in Poecilia reticulata. Evolution 34, 76–91 (1980)

  15. 15

    Godin, J.-G. J. & McDonough, H. E. Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav. Ecol. 14, 194–200 (2003)

  16. 16

    Farr, J. A. Male rarity or novelty, female choice behavior and sexual selection in the guppy Poecilia reticulata Peters (Pices: Poeciliidae). Evolution 31, 162–168 (1977)

  17. 17

    Hughes, K. A., Du, L., Rodd, F. H. & Reznick, D. N. Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Anim. Behav. 58, 907–916 (1999)

  18. 18

    Brooks, R. Negative genetic correlation between male sexual attractiveness and survival. Nature 406, 67–70 (2000)

  19. 19

    Jones, J. S., Leith, B. H. & Rawlings, P. Polymorphism in Cepaea: a problem with too many solutions? Annu. Rev. Ecol. Syst. 8, 109–143 (1977)

  20. 20

    Oxford, G. S. & Gillespie, R. G. Evolution and ecology of spider coloration. Annu. Rev. Entomol. 43, 619–643 (1998)

  21. 21

    Sinervo, B., Svensson, E. & Comendant, T. Density cycles and an offspring quantity and quality game driven by natural selection. Nature 406, 985–988 (2000)

  22. 22

    Rodd, F. H. & Reznick, D. N. Life-history evolution in guppies: III. The impact of prawn predation on guppy life histories. Oikos 62, 13–19 (1991)

  23. 23

    Reznick, D. N., Butler, M. J. 4th, Rodd, F. H. & Ross, P. Life-history evolution in guppies (Poecilia reticulata): 6. Differential mortality as a mechanism for natural selection. Evolution 50, 1651–1660 (1996)

  24. 24

    Bryant, M. J. & Reznick, D. Comparative studies of senescence in natural populations of guppies. Am. Nat. 163, 55–68 (2004)

  25. 25

    Endler, J. A. A predator's view of animal color patterns. Evol. Biol. 11, 319–364 (1978)

  26. 26

    Farr, J. A. Social behaviour patterns as determinants of reproductive success in the guppy, Poecilla reticulata Peters (Pisces, Poeciliidae). An experimental study of the effects of intermale competition, female choice, and sexual selection. Behaviour 74, 38–91 (1980)

  27. 27

    Bond, A. B. & Kamil, A. C. Visual predators select for crypticity and polymorphism in virtual prey. Nature 415, 609–613 (2002)

  28. 28

    Punzalan, D., Rodd, F. H. & Hughes, K. A. Perceptual processes and the maintenance of polymorphism through frequency-dependent predation. Evol. Ecol. 19, 303–320 (2005)

  29. 29

    Littell, R. C., Stroup, W. W. & Freund, R. J. SAS for Linear Models (SAS Institute, Cary, North Carolina, 2002)

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We thank C. Baril, M. Bryant, G. Cleven, K. Dixon, T. Hibler, A. Inman and T. Pitcher for help with field work; M. Bryant for advice on field experiments; Z. Columber, G. Chappel and K. Van Meter for help with scoring survival; and J. Burns, K. Dixon, M. Fitzpatrick, J. Leips, A. Price and C. Weadick for comments on the manuscript. This work was supported by grants from the National Science Foundation (to K.A.H. and A.E.H., and to D.N.R.) and by an NSERC grant to F.H.R. During 1996, K.A.H. was supported by an NIH NRSA Fellowship, and F.H.R. by the Center for Population Biology at the University of California at Davis. We thank the government of Trinidad and Tobago, and the Water and Sewage Authority, for permission to collect fish and conduct research. Author Contributions All authors collected field data. K.A.H., F.H.R. and A.E.H. designed the experiment. K.A.H. and F.H.R. supervised the field work. D.P. conducted reliability analysis; R.O. scored survival; and R.O. and K.A.H. analysed the data and wrote the manuscript. All authors discussed and commented on the manuscript, and suggested revisions.

Author information


  1. School of Integrative Biology

    • Robert Olendorf
    •  & Kimberly A. Hughes
  2. Institute for Genome Biology, University of Illinois, Urbana, Illinois, 61801, USA

    • Kimberly A. Hughes
  3. Department of Zoology, University of Toronto, Toronto, Ontario, M5S 3G5, Canada

    • F. Helen Rodd
    •  & David Punzalan
  4. Department of Biology, Lake Forest College, Lake Forest, Illinois, 60045, USA

    • Anne E. Houde
  5. Naos Marine Laboratory, Smithsonian Tropical Research Institute, Panama City, Roosvelt Avenue, APO AA 34002, Panama

    • Carla Hurt
  6. Department of Biology, University of California, Riverside, California, 92521, USA

    • David N. Reznick


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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Corresponding author

Correspondence to Kimberly A. Hughes.

Supplementary information

  1. Supplementary Notes

    This file contains Supplementary Tables 1–3, Supplementary Methods and Supplementary Notes. The Supplementary Tables report the release and recapture data and number of marked migrants identified at each site and year, and the results of analyses conducted to test for various sources of bias in the data collection and analysis. The Supplementary Methods contains details of definition and assignment of colour morphs, and of the evaluation of the reliability of morph classification. Supplementary Notes contains details on parametric analyses of recapture rates, on the evaluation of potential bias due to random assignment of males to home pools, and the GPS coordinates of the three sites used in our experiment. (RTF 423 kb)

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