1. School of Integrative Biology and
2. Institute for Genome Biology, University of Illinois, Urbana, Illinois 61801, USA
3. Department of Zoology, University of Toronto, Toronto, Ontario M5S 3G5, Canada
4. Department of Biology, Lake Forest College, Lake Forest, Illinois 60045, USA
5. Smithsonian Tropical Research Institute, Naos Marine Laboratory, Roosvelt Avenue (APO AA 34002), Panama City, Panama
6. Department of Biology, University of California, Riverside, California 92521, USA

Correspondence to: Kimberly A. Hughes^1,2 Correspondence and requests for materials should be addressed to K.A.H. (Email: kahughes@life.uiuc.edu).

The maintenance of genetic variation in traits under natural selection is a long-standing paradox in evolutionary biology^{1, 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 humans^{6, 7} and other species^{8, 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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