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.
Your institute does not have access to this article
Open Access articles citing this article.
Genomic and morphological data shed light on the complexities of shared ancestry between closely related duck species
Scientific Reports Open Access 17 June 2022
Body mass and geographic distribution determined the evolution of the wing flight-feather molt strategy in the Neornithes lineage
Scientific Reports Open Access 03 November 2021
Scientific Reports Open Access 24 September 2021
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Darwin, C. The Descent of Man, and Selection in Relation to Sex (John Murray, 1871)
Bateman, A. J. Intra-sexual selection in Drosophila. Heredity 2, 349–368 (1948)
Trivers, R. in Sexual Selection and the Descent of Man 1871–1971 (ed. Campbell, B. ) 136–179 (Aldine, 1972)
Andersson, M. B. Sexual Selection (Princeton Univ. Press, 1994)
Amundsen, T. Why are female birds ornamented? Trends Ecol. Evol. 15, 149–155 (2000)
Rubenstein, D. R. & Lovette, I. J. Reproductive skew and selection on female ornamentation in social species. Nature 462, 786–789 (2009)
Tobias, J. A., Montgomerie, R. & Lyon, B. E. The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Phil. Trans. R. Soc. B. 367, 2274–2293 (2012)
Lande, R. in Sexual Selection: Testing the Alternatives (eds Bradbury, J. W. & Andersson, M. ) 83–94 (Wiley, 1987)
Bonduriansky, R. & Chenoweth, S. F. Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288 (2009)
Kraaijeveld, K. Reversible trait loss: the genetic architecture of female ornaments. Annu. Rev. Ecol. Evol. Syst. 45, 159–177 (2014)
Poissant, J., Wilson, A. J. & Coltman, D. W. Sex-specific genetic variance and the evolution of sexual dimorphism: a systematic review of cross-sex genetic correlations. Evolution 64, 97–107 (2010)
Potti, J. & Canal, D. Heritability and genetic correlation between the sexes in a songbird sexual ornament. Heredity 106, 945–954 (2011)
Cardoso, G. C. & Mota, P. G. Evolution of female carotenoid colouration by sexual constraint in Carduelis finches. BMC Evol. Biol. 10, 82 (2010)
West-Eberhard, M. J. Sexual selection, social competition, and speciation. Q. Rev. Biol. 58, 155–183 (1983)
Lyon, B. E., Eadie, J. M. & Hamilton, L. D. Parental choice selects for ornamental plumage in American coot chicks. Nature 371, 240–243 (1994)
West-Eberhard, M. J. Darwin’s forgotten idea: the social essence of sexual selection. Neurosci. Biobehav. Rev. 46, 501–508 (2014)
Lyon, B. E. & Montgomerie, R. Sexual selection is a form of social selection. Phil. Trans. R. Soc. B. 367, 2266–2273 (2012)
del Hoyo, J., Elliott, A. & Christie, D. A. Handbook of the Birds of the World Vols 8–16 (Lynx Edicions, 2003–2011)
Badyaev, A. V. & Hill, G. E. Avian sexual dichromatism in relation to phylogeny and ecology. Annu. Rev. Ecol. Evol. Syst. 34, 27–49 (2003)
Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010)
von Hardenberg, A. & Gonzalez-Voyer, A. Disentangling evolutionary cause-effect relationships with phylogenetic confirmatory path analysis. Evolution 67, 378–387 (2013)
Galván, I., Negro, J. J., Rodríguez, A. & Carrascal, L. M. On showy dwarfs and sober giants: body size as a constraint for the evolution of bird plumage colouration. Acta Ornithol. 48, 65–80 (2013)
Ricklefs, R. E. Insights from comparative analyses of aging in birds and mammals. Aging Cell 9, 273–284 (2010)
Stutchbury, B. J. & Morton, E. S. Behavioral Ecology of Tropical Birds (Academic, 2001)
Bailey, S. F. Latitudinal gradients in colors and patterns of passerine birds. Condor 80, 372–381 (1978)
Tobias, J. A., Gamarra-Toledo, V., García-Olaechea, D., Pulgarín, P. C. & Seddon, N. Year-round resource defence and the evolution of male and female song in suboscine birds: social armaments are mutual ornaments. J. Evol. Biol. 24, 2118–2138 (2011)
Irwin, R. E. The evolution of plumage dichromatism in the New World blackbirds: social selection on female brightness. Am. Nat. 144, 890–907 (1994)
Kokko, H. & Johnstone, R. A. Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Phil. Trans. R. Soc. B. 357, 319–330 (2002)
Emlen, S. T. & Oring, L. W. Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223 (1977)
Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012)
Valcu, M. & Dale, J. colorZapper: color extraction utilities. R package version 1.0. https://github.com/valcu/colorZapper (2014)
Craig, A. in Handbook of the Birds of the World Vol. 15 (eds Del Hoyo, J., Elliot, A. & Christie, D. A. ) (Lynx Edicions, 2010)
Starck, J. M. Review of Handbook of the Birds of the World. Ethology 102, 436–440 (1996)
Badyaev, A. V. & Hill, G. E. Evolution of sexual dichromatism: contribution of carotenoid-versus melanin-based colouration. Biol. J. Linn. Soc. 69, 153–172 (2000)
Gray, D. A. Carotenoids and sexual dichromatism in North American passerine birds. Am. Nat. 148, 453–480 (1996)
Owens, I. P. F. & Hartley, I. R. Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proc. R. Soc. Lond. B 265, 397–407 (1998)
Olson, V. A. & Owens, I. P. F. Interspecific variation in the use of carotenoid-based colouration in birds: diet, life history and phylogeny. J. Evol. Biol. 18, 1534–1546 (2005)
Dey, C. J., Valcu, M., Kempenaers, B. & Dale, J. Carotenoid-based bill coloration functions as a social, not sexual, signal in songbirds (Aves: Passeriformes). J. Evol. Biol. 28, 250–258 (2015)
Seddon, N., Tobias, J. A., Eaton, M. & Odeen, A. Human vision can provide a valid proxy for avian perception of sexual dichromatism. Auk 127, 283–292 (2010)
Cuthill, I. C. in Bird Colouration, Volume 1: Mechanisms and Measurements (eds Hill, G. E. & McGraw, K. J. ) 3–40 (Harvard Univ. Press, 2006)
Dale, J. et al. Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism. Proc. R. Soc. B 274, 2971–2979 (2007)
Calder, W. A. Size, Function, and Life History (Courier Corporation, 1996)
Pianka, E. R. On r- and K-selection. Am. Nat. 104, 592–597 (1970)
Hofmann, C. M., Cronin, T. W. & Omland, K. E. Evolution of sexual dichromatism. 1. Convergent losses of elaborate female colouration in New World orioles (Icterus spp.). Auk 125, 778–789 (2008)
Price, J. J. & Eaton, M. D. Reconstructing the evolution of sexual dichromatism: current color diversity does not reflect past rates of male and female change. Evolution 68, 2026–2037 (2014)
Burns, K. J. A phylogenetic perspective on the evolution of sexual dichromatism in tanagers (Thraupidae): the role of female versus male plumage. Evolution 52, 1219–1224 (1998)
Johnson, A. E., Jordan Price, J. & Pruett-Jones, S. Different modes of evolution in males and females generate dichromatism in fairy-wrens (Maluridae). Ecol. Evol. 3, 3030–3046 (2013)
Dunn, P. O., Armenta, J. K. & Whittingham, L. A. Natural and sexual selection act on different axes of variation in avian plumage color. Sci. Adv. 1, e1400155 (2015)
Rubenstein, D. R. Sexual and social competition: broadening perspectives by defining female roles. Phil. Trans. R. Soc. B. 367, 2248–2252 (2012)
Alerstam, T., Hedenström, A. & Åkesson, S. Long-distance migration: evolution and determinants. Oikos 103, 247–260 (2003)
Simpson, R. K., Johnson, M. A. & Murphy, T. G. Migration and the evolution of sexual dichromatism: evolutionary loss of female colouration with migration among wood-warblers. Proc. R. Soc. B 282, 20150375 (2015)
Fitzpatrick, S. Colourful migratory birds: evidence for a mechanism other than parasite resistance for the maintenance of ‘good genes’ sexual selection. Proc. R. Soc. Lond. B 257, 155–160 (1994)
Dunning, J. B. CRC Handbook of Avian Body Masses 2nd edn (CRC, 2008)
Valcu, M., Dale, J. & Kempenaers, B. rangeMapper: a platform for the study of macroecology of life-history traits. Glob. Ecol. Biogeogr. 21, 945–951 (2012)
Land Processes Distributed Active Archive Center (LP DAAC). MODIS/Terra Land Surface Temperature/Emissivity 8-Day L3 Global 0.05Deg (LP DAAC, 2014)
Marchant, S. & Higgins, P. J. Handbook of Australian, New Zealand & Antarctic Birds (Oxford Univ. Press, 1990–2006)
Cramp, S. & Simmons, K. E. L. Handbook of the Birds of Europe, the Middle East and North Africa: the Birds of the Western Palearctic (Oxford Univ. Press, 1977–1994)
Brown, L. H., Urban, E. K. & Newmann, K. The Birds of Africa (Academic, 1982–2004)
Hockey, P. A. R., Dean, W. R. J. & Ryan, P. G. Roberts — Birds of Southern Africa 7th edn (John Voelcker Bird Book Fund, 2005)
Poole, A. & Gill, F. Birds of North America (Cornell Lab of Ornithology, 1992–2003)
Dunn, P. O., Whittingham, L. A. & Pitcher, T. E. Mating systems, sperm competition, and the evolution of sexual dimorphism in birds. Evolution 55, 161–175 (2001)
Pitcher, T. E., Dunn, P. O. & Whittingham, L. A. Sperm competition and the evolution of testes size in birds. J. Evol. Biol. 18, 557–567 (2005)
Cockburn, A. Prevalence of different modes of parental care in birds. Proc. R. Soc. B 273, 1375–1383 (2006)
Martins, E. P. & Hansen, T. F. Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149, 646–667 (1997)
Freckleton, R. P., Harvey, P. H. & Pagel, M. Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726 (2002)
Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999)
Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008)
Garland, T. Jr & Ives, A. R. Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. Am. Nat. 155, 346–364 (2000)
Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004)
Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D. nlme: Linear and nonlinear mixed effects models. R package version 3.1–117. http://CRAN.R-project.org/package=nlme (2014)
Revell, L. J. Phylogenetic signal and linear regression on species data. Methods Ecol. Evol. 1, 319–329 (2010)
Revell, L. J. Size-correction and principal components for interspecific comparative studies. Evolution 63, 3258–3268 (2009)
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012)
R Core Team. R: A language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014)
Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010)
Bartoszek, K., Pienaar, J., Mostad, P., Andersson, S. & Hansen, T. F. A phylogenetic comparative method for studying multivariate adaptation. J. Theor. Biol. 314, 204–215 (2012)
Beaulieu, J. M., Jhwueng, D. C., Boettiger, C. & O’Meara, B. C. Modeling stabilizing selection: expanding the Ornstein-Uhlenbeck model of adaptive evolution. Evolution 66, 2369–2383 (2012)
Hansen, T. F. in Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (ed. Garamszegi, L. Z. ) 351–379 (Springer, 2014)
Clavel, J., Escarguel, G. & Merceron, G. mvMORPH: an R package for fitting multivariate evolutionary models to morphometric data. Meth. Ecol. Evol. http://dx.doi.org/10.1111/2041-210X.12420 (2015)
Shipley, B. A new inferential test for path models based on directed acyclic graphs. Struct. Equ. Modeling 7, 206–218 (2000)
Shipley, B. Cause and Correlation in Biology: a User’s Guide to Path Analysis, Structural Equations and Causal Inference (Cambridge Univ. Press, 2002)
Gonzalez-Voyer, A. & von Hardenberg, A. in Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (ed. Garamszegi, L. Z. ) 201–229 (Springer, 2014)
Shipley, B. The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology 94, 560–564 (2013)
Arnold, T. W. Uninformative parameters and model selection using Akaike’s information criterion. J. Wildl. Mgmt. 74, 1175–1178 (2010)
Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002)
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.
The authors declare no competing financial interests.
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. c–h, 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.
a–n, Arrows indicate hypothesized direct links between variables.
About this article
Cite this article
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
Genomic and morphological data shed light on the complexities of shared ancestry between closely related duck species
Scientific Reports (2022)
Nature Ecology & Evolution (2022)
Behavioral Ecology and Sociobiology (2022)
No evidence for potential sexual information from a monochromatic carotenoid trait in a dichromatic woodpecker species
Journal of Ornithology (2022)