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The effects of life history and sexual selection on male and female plumage colouration

Abstract

Classical sexual selection theory1,2,3,4 provides a well-supported conceptual framework for understanding the evolution and signalling function of male ornaments. It predicts that males obtain greater fitness benefits than females through multiple mating because sperm are cheaper to produce than eggs. Sexual selection should therefore lead to the evolution of male-biased secondary sexual characters. However, females of many species are also highly ornamented5,6,7. The view that this is due to a correlated genetic response to selection on males1,8 was widely accepted as an explanation for female ornamentation for over 100 years5 and current theoretical9,10 and empirical11,12,13 evidence suggests that genetic constraints can limit sex-specific trait evolution. Alternatively, female ornamentation can be the outcome of direct selection for signalling needs7,14. Since few studies have explored interspecific patterns of both male and female elaboration, our understanding of the evolution of animal ornamentation remains incomplete, especially over broad taxonomic scales. Here we use a new method to quantify plumage colour of all ~6,000 species of passerine birds to determine the main evolutionary drivers of ornamental colouration in both sexes. We found that conspecific male and female colour elaboration are strongly correlated, suggesting that evolutionary changes in one sex are constrained by changes in the other sex. Both sexes are more ornamented in larger species and in species living in tropical environments. Ornamentation in females (but not males) is increased in cooperative breeders—species in which female–female competition for reproductive opportunities and other resources related to breeding may be high6. Finally, strong sexual selection on males has antagonistic effects, causing an increase in male colouration but a considerably more pronounced reduction in female ornamentation. Our results indicate that although there may be genetic constraints to sexually independent colour evolution, both female and male ornamentation are strongly and often differentially related to morphological, social and life-history variables.

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Figure 1: Interspecific variation in avian plumage colouration.
Figure 2: The method used for quantifying plumage colouration.
Figure 3: Plumage scores and plumage dichromatism in relation to key predictors in passerine birds.
Figure 4: Coefficient estimates and model lines of linear mixed models predicting plumage scores in 2,471 species of passerines.
Figure 5: Relationships among ecological variables and plumage colouration, as determined by phylogenetic controlled d separation path analysis21.

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Acknowledgements

We thank the many ornithologists and scientists who have published their data or contributed data to public databases, allowing us to conduct this study. Thanks to J. D. Aguirre, P. M. Buston, J. Clavel, P. B. Rainey, L. Redfern and J. A. Tobias for comments on manuscript drafts and to the staff of Museum Victoria and the Australian National Wildlife Collection for access to museum specimens. This work was supported by Massey University and a grant from the Australian and Pacific Science Foundation (APSF 10/8) to J.D. C.J.D. was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Canadian Graduate Scholarship. K.D. was supported by the Australian Research Council (DE120102323). B.K. and M.V. were generously supported by the Max Planck Society.

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Authors and Affiliations

Authors

Contributions

Conceived of the study: J.D., M.V. and B.K.; collected the data: J.D., M.V., K.D. and C.J.D.; developed the methods: J.D. and M.V.; analysed the data: J.D. and C.J.D. with help from M.V. and K.D.; wrote the paper: J.D. and C.J.D. with input from the other authors.

Corresponding author

Correspondence to James Dale.

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The authors declare no competing financial interests.

Additional information

Data sets have been deposited in the Dryad Digital Repository (http://dx.doi.org/10.5061/dryad.1rp0s).

Extended data figures and tables

Extended Data Figure 1 Comparison of plumage scores determined with handbook plates in RGB colour space with plumage scores determined with study skins using UV–Vis spectrometry.

a, RGB versus UV–Vis scores calculated with 534 Australian bird species (reduced major axis (RMA) regression: y = 0.965x + 2.025, N = 1068, R2 = 0.670, P < 0.0001). b, PGLS model effect sizes determined with RGB scores versus effect sizes determined with UV–Vis scores (RMA regression: y = 0.878x − 0.042, N = 30 model effects, R2 = 0.809, P < 0.0001, each model had 305 Australian passerine species in it and black, red and green points reflect models predicting female scores, male scores and dichromatism scores, respectively). c, MCMCglmm model effect sizes (including interaction effects) determined with RGB versus UV–Vis scores (RMA regression: y = 0.991x − 0.028, R2 = 0.930, P < 0.0001, N = 11 effects, the model had 305 Australian passerine species in it and each point reflects the mean effect size calculated from five models using a separate phylogenetic tree from http://birdtree.org each).

Extended Data Figure 2 Basic patterns of plumage colouration in the order Passeriformes (N = 5,983 species).

a, Male versus female patch scores (upper breast shown as an example). Data points are coloured by the male RGB values scored from handbook plates. b, As in a, only points are coloured with female RGB scores. ch, The colours associated with different plumage scores differentiated by patch type. The y axis is a normally distributed random number used to spread out variation and improve visualization. The figure reflects patterns that agree with our intuition: dull greens, olives and browns have low plumage scores (are female-like), while richer or high contrasting colours (blacks, purples, blues, reds and yellows) have high scores (are male-like).

Extended Data Figure 3 MCMCglmm results are robust to various cut-offs used to determine plumage scores.

a, b, Main effects (a) and interaction (b) with sex effects. Filled circles: estimates where P < 0.001; open circles: estimates where 0.05 > P > 0.001. The vertical line represents the cut-off value used in the main analysis. To reduce processing time for this analysis each MCMCglmm model ran for 10,000 iterations with a sampling interval of 100. Parameter estimates from the shortened runs were highly similar to the parameter estimates reported in the main MCMCglmm analysis (see Extended Data Table 4). Note that the observed decline in effect sizes as the cut-off size increases is the automatic outcome of how plumage scores are calculated. As the cut-off size approaches 100% the variance in plumage scores necessarily approaches 0 and so the effect sizes will inevitably also approach 0.

Extended Data Figure 4 Candidate models for phylogenetic confirmatory path analysis.

an, Arrows indicate hypothesized direct links between variables.

Extended Data Table 1 Comparison of multivariate co-evolutionary models of male and female plumage ornamentation
Extended Data Table 2 Phylogenetic generalized least-squares models on predictors of sexual dichromatism in the Passeriformes
Extended Data Table 3 Phylogenetic principal component analysis loadings and the variance explained by each component
Extended Data Table 4 Morphological, life-history and social correlates of plumage colour scores in passerine birds (N = 2,471 species)
Extended Data Table 5 Comparison of models used in phylogenetic confirmatory path analysis

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Dale, J., Dey, C., Delhey, K. et al. The effects of life history and sexual selection on male and female plumage colouration. Nature 527, 367–370 (2015). https://doi.org/10.1038/nature15509

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