Mating advantage for rare males in wild guppy populations

Abstract

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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Figure 1: Colour pattern variation among males from a single population.
Figure 2: Rare colour patterns have higher mating and reproductive success.

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Acknowledgements

We thank R. Olendorf for help with field work and genotyping; D. Punzalan, K. Dixon, M. Bryant, T. Pitcher, C. Baril, A. Inman and C. Hurt for field work; C. Gibson, K. McGhee for photographs in Fig. 1 and for animal rearing; J. Koprivnikar for animal rearing; and A. Vanesyan for collecting morphology data. D. Reznick provided advice on field experiments, and D. Punzalan, K. Dixon and M. Fitzpatrick commented on manuscript drafts. In Trinidad, we thank the Sinanan family for accommodation, and I. Ramnarine and the government of Trinidad for permission to collect guppies and to work in the Quare watershed. This work was supported by grants from the National Science Foundation (to K.A.H. and A.E.H.) and the Natural Sciences and Engineering Research Council (NSERC) of Canada (to F.H.R.).

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Authors

Contributions

K.A.H. and F.H.R conceived and designed the experiment and conducted all data analyses. A.E.H. consulted on experimental design and A.C.P reared live animals. All authors participated in field experiments and in writing the paper.

Corresponding author

Correspondence to Kimberly A. Hughes.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Population means for effects of rarity and morph on reproductive success.

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 Table 1 Effect of experimental factors and quantitative traits on reproductive success in first-brood offspring
Extended Data Table 2 Effect of experimental factors and quantitative traits on reproductive success
Extended Data Table 3 Population-specific estimates of the association between area of orange body colour and reproductive success
Extended Data Table 4 Effect of experimental factors and quantitative traits on reproductive success
Extended Data Table 5 Parameter estimates for effects of morph (coloured – uncoloured) and the area of orange body colour, on number of assigned mates and assigned offspring

Supplementary information

Supplementary Table 1

The table contains the following data: Experimental males, classification, phenotypes, and assigned offspring and mates. (XLSX 81 kb)

Supplementary Table 2

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. (XLSX 69 kb)

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Hughes, K., Houde, A., Price, A. et al. Mating advantage for rare males in wild guppy populations. Nature 503, 108–110 (2013). https://doi.org/10.1038/nature12717

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