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Deep learning reveals the complex genetic architecture of male guppy colouration

Nature Ecology & Evolution volume 9, pages 1614–1625 (2025)Cite this article

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Abstract

The extraordinary variation in male guppy (Poecilia reticulata) colouration is a powerful model for studying the interplay of natural and sexual selection. However, the complexity of this variation has hampered the high-resolution characterization and determination of the genetic architecture underlying male guppy colour and clouded our understanding of how this exceptional level of diversity is maintained. Here we identify the heritability and genetic basis of male colour variation using convolutional neural networks for high-resolution phenotyping coupled with selection experiments, controlled pedigrees and whole-genome resequencing for a genome-wide association study of colour traits. Our phenotypic and genomic results converge to show that colour patterning in guppies is a combination of many heritable features, each with a largely independent genetic architecture spanning the entire genome. Autosomally inherited ornaments are polygenic, with significant contributions from loci involved in neural crest cell migration. Unusually, the results of our genome-wide association study suggest that gene duplicates from the autosomes to the Y chromosome are responsible for much of the sex-linked variation in colour in guppies, providing a potential mechanism for the maintenance of variation of this classic model trait.

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Fig. 1: Quantification of pattern variation.
Fig. 2: Orange colour responds rapidly to selection.
Fig. 3: The localized heritability of colour is high, but the architecture is heterogeneous.
Fig. 4: Orange ornaments are strongly heritable, and their incidence and size responded to selection.
Fig. 5: The genetic architecture of colour pattern is a mix of autosomal loci and sex-linked loci.
Fig. 6: Large-effect CNVs underlie sex-linked variation in colour pattern.

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Data availability

Sequence data are available via the SRA under accession PRJNA1262490 (http://www.ncbi.nlm.nih.gov/bioproject/1262490), image data are available via the Federated Research Data Repository94 and tabular data are available via Zenodo at https://doi.org/10.5281/zenodo.15499676 (ref. 19). Source data are provided with this paper.

Code availability

Code is available via GitHub at https://github.com/Ax3man/vdBijl_etal_2025_GuppyColorPatterns and via Zenodo at https://doi.org/10.5281/zenodo.15499676 (ref. 19).

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Acknowledgements

We thank L. Yong for sharing insights on guppy photography. We thank B. Sandkam, B. Furman, D. Metzger, L. Fong, Y. Lin, C. Hodson and J. Lewis for help with animal husbandry and valuable discussions and T. Booker for advice and comments on an earlier draft. Y. Lin contributed the female coverage data. Funding was provided by a Canada 150 Research Chair, NSERC and an ERC grant (680951) to J.E.M.

Author information

Authors and Affiliations

  1. Department of Zoology, Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada

    Wouter van der Bijl, Jacelyn J. Shu, Versara S. Goberdhan, Linley M. Sherin, Changfu Jia, Maria Cortazar-Chinarro, Alberto Corral-Lopez & Judith E. Mank

  2. Division of Ecology and Genetics, Uppsala University, Uppsala, Sweden

    Maria Cortazar-Chinarro & Alberto Corral-Lopez

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  1. Wouter van der Bijl
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  2. Jacelyn J. Shu
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  3. Versara S. Goberdhan
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  6. Maria Cortazar-Chinarro
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  7. Alberto Corral-Lopez
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Contributions

Conceptualization: W.v.d.B., A.C.-L. and J.E.M.; methodology: W.v.d.B.; formal analysis: W.v.d.B. and A.C.-L.; investigation: W.v.d.B., J.J.S., V.S.G., L.M.S., C.J., M.C.-C., A.C.-L. and J.E.M.; writing—original draft: W.v.d.B. and J.E.M.; writing—review and editing: W.v.d.B., J.J.S., V.S.G., L.M.S., C.J., M.C.-C., A.C.-L. and J.E.M.; visualization: W.v.d.B.; supervision: J.E.M.; project administration: J.J.S.; funding acquisition: J.E.M.

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Correspondence to Wouter van der Bijl.

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Nature Ecology & Evolution thanks Nidal Karagic, Claudius Kratochwil and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Variance components and heritability of total color, as estimated by a Bayesian animal model.

a) Cumulative posterior density bar graphs, for each component of total orange (left) and black (right) color. Bars represent in order: autosomal, X-linked and Y-linked genetic variance, maternal effects variance, tank environment variance, other environmental variance, variance due to asymmetry, and measurement error. b) Posterior distributions of the total, X-linked and Y-linked heritability of total color. c) Posterior distributions of the correlation between orange and black variance components. Posterior summaries are shown as posterior means (point) and 66% (thick lines) and 95% (thin lines) credible intervals in all panels.

Source data

Extended Data Fig. 2 Correlated effects of selection on orange area on the incidence of black coloration.

a) Density plots show the distribution of the percent of black coloration per generation and selection regime. Thin lines between generations connect fathers and sons. Thick lines inside the densities show the median value of color area. b) Heatmaps illustrating the effect of selection across the body. Each heatmap cell is colored by the log odds ratio (as estimated by a generalized linear mixed model), illustrating the relative odds that a male has black color at that location. Body positions where the incidence of black color is less than 1% are colored grey. c) Effect of selection on orange on location in black patternspace. Axes show black patternspace (after UMAP dimension reduction), with points indicating individuals, colored by selection direction, and facets showing the four generations.

Source data

Extended Data Fig. 3 Effects of artificial selection for orange coloration on sexual behavior, gross morphology and life history.

a to e) Comparison of display and sexually coercive behavior between down-selected (n = 46) and up-selected (n = 49) males from the F3 generation. f to h) Comparison of gross morphology between down-selected (n = 63) and up-selected (n = 62) males from the F3 generation. i & j) Comparison for life history parameters between down-selected (nF1 = 106, nF2 = 106) and up-selected (nF1 = 104, nF2 = 105) females from the F1 and F2 generations. All panels: Violin plots show the kernel densities of observations, and point estimates and error bars show the point estimate and 95% confidence intervals for the groups means estimated by a linear mixed model.

Source data

Extended Data Fig. 4 Black ornaments are heritable but responded only weakly to selection on orange color.

a) Pictograms of eight black ornaments. b) Heritabilities of the incidence and size (when present) of each ornament. Dots and lines reflect point estimates and 95% credible intervals, and the gradient bars show the cumulative posterior density. c&d) Effect of selection on the incidence and size of black ornaments. Error bars show 95% bootstrapped confidence intervals, and points represent means. X-axes show consecutive generations. Sample size (number of fish); P generation: 300; down-selected F1, F2, F3: 453, 570, 441; up-selected F1, F2, F3: 508, 513, 444.

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Extended Data Fig. 5 Top 30 most common ornament combinations.

The y-axis shows the median color pattern for each combination of ornaments, while x-axis shows its count (top) and frequency in the population (bottom). The bars indicate the observed frequency, while the orange lines show the frequency predicted from the incidence of each of the pattern’s ornaments. Inset: The number of unique ornament combinations in the full dataset of all males (black line), compared the expectation derived from ornament incidence (orange). The expected distribution was calculated by randomly generating 3,229 males and their ornaments with P(incidence), repeated 1,000 times. The point and errorbar denote the mean and 95% confidence interval.

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Extended Data Fig. 6 Pattern space encodes variation in the incidence and size of ornaments.

a&c) Pictograms of seven orange and eight black ornaments, matching with the associated panels in B&D respectively. b&d) Axes are the UMAP reduced representation of five-dimensional pattern space. Individuals are colored by the size of their relevant ornament, expressed as a fraction of the largest observed size, or colored grey if they lack the ornament. Note the use of a logarithmic scale for ornament size.

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Extended Data Fig. 7 GWAS results for the presence/absence of six orange ornaments, as in Fig. 5.

Points represent SNPs and small indels, with their genomic location on the x-axis, and the p-value of the association on the y-axis. Numbers along the x axis denote linkage groups. Sex-linked loci are placed to the side, with both the sex-chromosome (LG12) and sex-linked loci cross-mapping to the autosomes shown, colored by their putative origin (red = X, blue = Y). Peaks are labelled with gene names, but unnamed and uncharacterized genes are not shown. Names with asterisk (*) indicate that more significant cross-mapping SNPs were present in the same peak.

Extended Data Fig. 8 GWAS results for the presence/absence of six black ornaments, as in Fig. 5.

Points represent SNPs and small indels, with their genomic location on the x-axis, and the p-value of the association on the y-axis. Numbers along the x axis denote linkage groups. Sex-linked loci are placed to the side, with both the sex-chromosome (LG12) and sex-linked loci cross-mapping to the autosomes shown, colored by their putative origin (red = X, blue = Y). Peaks are labelled with gene names, but unnamed and uncharacterized genes are not shown. Names with asterisk (*) indicate that more significant cross-mapping SNPs were present in the same peak.

Extended Data Fig. 9 Autosomally inherited ornaments are complex traits.

a) Pictograms of eight ornaments with (partial) autosomal inheritance. b) Illustrative GWAS peaks for the association with the ornaments depicted in A. Each point is a genetic variant, with black points surpassing the FDR-threshold, and the red point is the top variant. Horizontal lines show the location of all annotated genes, with labels only shown for characterized genes. c) Bars indicate the proportion of individuals with the ornament (depicted in A) depending on their genotype at the top variant. The proportion of variation in the phenotype that is explained by the top variant is displayed as Nagelkerke’s R2 calculated from a logistic regression. d) PheWAS heatmaps displaying Z-scores for the effect of the top variant on orange or black color across the body, controlling for autosomal and sex-linked relatedness.

Extended Data Fig. 10 Expression at texim and relation to ornament O6.

a) Expression of texim copy 6531 in three male and three female pools, as counts per million (CPM). b) The proportion of males with ornament O6, as a function of the presence of texim copy 6531, as determined by reads with diagnostic SNPs for that copy. The proportion of phenotypic variance is shown as Nagelkerke’s R2.

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Supplementary Notes, Figs. 1–14 and Table 1.

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Source Data Figs. 1–6

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Source Data Extended Data Figs. 1–6 and 10

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van der Bijl, W., Shu, J.J., Goberdhan, V.S. et al. Deep learning reveals the complex genetic architecture of male guppy colouration. Nat Ecol Evol 9, 1614–1625 (2025). https://doi.org/10.1038/s41559-025-02781-w

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