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Frequency-dependent survival in natural guppy populations

Abstract

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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Figure 1: Males before release and after recapture.
Figure 2: Relative recapture rates for rare and common phenotypes.

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Acknowledgements

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.

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Correspondence to Kimberly A. Hughes.

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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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Olendorf, R., Rodd, F., Punzalan, D. et al. Frequency-dependent survival in natural guppy populations. Nature 441, 633–636 (2006). https://doi.org/10.1038/nature04646

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