Mating advantage for rare males in wild guppy populations

Journal name:
Nature
Volume:
503,
Pages:
108–110
Date published:
DOI:
doi:10.1038/nature12717
Received
Accepted
Published online

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.

At a glance

Figures

  1. Colour pattern variation among males from a single population.
    Figure 1: Colour pattern variation among males from a single population.

    Male offspring of Quare River 7 tributary fish, reared in a common environment and showing heritable colour-pattern variation. Males on the left have a caudal fin that is representative of the ‘uncoloured’ group, those on right are have a caudal fin that is representative of the ‘coloured’ group. Criteria for classification are described in ref. 9.

  2. Rare colour patterns have higher mating and reproductive success.
    Figure 2: Rare colour patterns have higher mating and reproductive success.

    a, Number of mates and offspring assigned to common (white, n = 124) or rare (dark grey, n = 42) males. Centre values are marginal means from the full generalized linear mixed model; bars indicate s.e.m. adjusted for model covariance parameters. **P <0.005 and *P = 0.01, respectively; see Extended Data Table 1. b, c, Association between square-root orange area and reproductive success in Quare River 7 (solid line, n = 34), Quare River 1 (dashed line, n = 72) and Mausica River (dotted line, n = 60), predicted from the full model. b, Predicted mates. c, Predicted offspring; see Extended Data Table 2. Minimum and maximum values along abcissa indicate range of values recorded.

  3. Population means for effects of rarity and morph on reproductive success.
    Extended Data Fig. 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, 19rare; 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.

Tables

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

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Author information

Affiliations

  1. Department of Biological Science, 319 Stadium Drive, Florida State University, Tallahassee, Florida 32306, USA

    • Kimberly A. Hughes
  2. Department of Biology, Lake Forest College, 555 North Sheridan Road, Lake Forest, Illinois 60045, USA

    • Anne E. Houde
  3. Department of Ecology and Evolutionary Biology, University of Toronto, 25 Harbord Street, Toronto, Ontario M5S 3G5, Canada

    • Anna C. Price &
    • F. Helen Rodd

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.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Author details

Extended data figures and tables

Extended Data Figures

  1. 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, 19rare; 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

  1. Extended Data Table 1: Effect of experimental factors and quantitative traits on reproductive success in first-brood offspring (821 KB)
  2. Extended Data Table 2: Effect of experimental factors and quantitative traits on reproductive success (792 KB)
  3. Extended Data Table 3: Population-specific estimates of the association between area of orange body colour and reproductive success (179 KB)
  4. Extended Data Table 4: Effect of experimental factors and quantitative traits on reproductive success (830 KB)
  5. 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 (271 KB)

Supplementary information

Excel files

  1. Supplementary Table 1 (81 KB)

    The table contains the following data: Experimental males, classification, phenotypes, and assigned offspring and mates.

  2. 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.

Additional data