To understand the processes that maintain genetic diversity is a long-standing challenge in evolutionary biology, with implications for predicting disease resistance, response to environmental change, and population persistence1, 2, 3. Simple population genetic models are not sufficient to explain the high levels of genetic diversity sometimes observed in ecologically important traits2. In guppies (Poecilia reticulata), male colour pattern is both diverse and heritable, and is arguably one of the most extreme examples of morphological polymorphism known4, 5. Negative frequency-dependent selection (NFDS), a form of selection in which genotypes are favoured when they are rare6, can potentially maintain such extensive polymorphism, but few experimental studies have confirmed its operation in nature7, 8. Here we use highly replicated experimental manipulations of natural populations to show that males with rare colour patterns have higher reproductive fitness, demonstrating NFDS mediated by sexual selection. Rare males acquired more mates and sired more offspring compared to common males and, as previously reported, had higher rates of survival8. Orange colour, implicated in other studies of sexual selection in guppies, did predict male reproductive success, but only in one of three populations. These data support the hypothesis that NFDS maintains diversity in the colour patterns of male guppies through two selective agents, mates and predators. Similar field-based manipulations of genotype frequencies could provide a powerful approach to reveal the underlying ecological and behavioural mechanisms that maintain genetic and phenotypic diversity.
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Extended data figures and tables
Extended Data Figures
- Extended Data Figure 1: Population means for effects of rarity and morph on reproductive success. (74 KB)
Centre values are marginal means from generalized linear mixed models; bars indicate s.e.m. adjusted for model parameters. *P < 0.01 and **P < 0.05, respectively. a, Mates assigned to common (white bars) and rare (dark grey bars) males in all populations (All, n = 124 common, 42 rare) and by population (M, Mausica, n = 43 common, 17 rare; Q1, Quare 1, n = 53 common, 19 rare; Q7, Quare 7, n = 28 common, 6 rare). b, Offspring for common and rare males. c, Mates assigned to males with uncoloured (white bars) or coloured (dark grey bars) tails for all populations (All, n = 79 uncoloured, 87 coloured) and by population (M, Mausica, n = 26 uncoloured, 34 coloured; Q1, Quare 1, n = 35 uncoloured, 37 coloured; Q7, Quare 7, n = 18 uncoloured, 16 coloured). d, Offspring for males with uncoloured and coloured tails.
Extended Data Tables
- Supplementary Table 1 (81 KB)
The table contains the following data: Experimental males, classification, phenotypes, and assigned offspring and mates.
- Supplementary Table 2 (69 KB)
This table contains the following data: Results of paternity analysis; number of loci scored for offspring, mother, and candidate father, number of mismatches, LOD (log odds ratio), delta scores, and Confidence category. Only offspring assigned to experimental 'rare' and 'common' males are listed.