Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

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.

References

  1. Darwin, C. The Descent of Man, and Selection in Relation to Sex (John Murray, 1871)

  2. Bateman, A. J. Intra-sexual selection in Drosophila. Heredity 2, 349–368 (1948)

    CAS  Article  PubMed  Google Scholar 

  3. Trivers, R. in Sexual Selection and the Descent of Man 1871–1971 (ed. Campbell, B. ) 136–179 (Aldine, 1972)

  4. Andersson, M. B. Sexual Selection (Princeton Univ. Press, 1994)

  5. Amundsen, T. Why are female birds ornamented? Trends Ecol. Evol. 15, 149–155 (2000)

    CAS  PubMed  Article  Google Scholar 

  6. Rubenstein, D. R. & Lovette, I. J. Reproductive skew and selection on female ornamentation in social species. Nature 462, 786–789 (2009)

    ADS  CAS  PubMed  Article  Google Scholar 

  7. 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)

    PubMed  Article  PubMed Central  Google Scholar 

  8. Lande, R. in Sexual Selection: Testing the Alternatives (eds Bradbury, J. W. & Andersson, M. ) 83–94 (Wiley, 1987)

  9. Bonduriansky, R. & Chenoweth, S. F. Intralocus sexual conflict. Trends Ecol. Evol. 24, 280–288 (2009)

    PubMed  Article  Google Scholar 

  10. Kraaijeveld, K. Reversible trait loss: the genetic architecture of female ornaments. Annu. Rev. Ecol. Evol. Syst. 45, 159–177 (2014)

    Article  Google Scholar 

  11. 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)

    PubMed  Article  Google Scholar 

  12. Potti, J. & Canal, D. Heritability and genetic correlation between the sexes in a songbird sexual ornament. Heredity 106, 945–954 (2011)

    CAS  PubMed  Article  Google Scholar 

  13. Cardoso, G. C. & Mota, P. G. Evolution of female carotenoid colouration by sexual constraint in Carduelis finches. BMC Evol. Biol. 10, 82 (2010)

    Google Scholar 

  14. West-Eberhard, M. J. Sexual selection, social competition, and speciation. Q. Rev. Biol. 58, 155–183 (1983)

    Article  Google Scholar 

  15. Lyon, B. E., Eadie, J. M. & Hamilton, L. D. Parental choice selects for ornamental plumage in American coot chicks. Nature 371, 240–243 (1994)

    ADS  Article  Google Scholar 

  16. West-Eberhard, M. J. Darwin’s forgotten idea: the social essence of sexual selection. Neurosci. Biobehav. Rev. 46, 501–508 (2014)

    PubMed  Article  Google Scholar 

  17. Lyon, B. E. & Montgomerie, R. Sexual selection is a form of social selection. Phil. Trans. R. Soc. B. 367, 2266–2273 (2012)

    PubMed  Article  PubMed Central  Google Scholar 

  18. del Hoyo, J., Elliott, A. & Christie, D. A. Handbook of the Birds of the World Vols 8–16 (Lynx Edicions, 2003–2011)

  19. Badyaev, A. V. & Hill, G. E. Avian sexual dichromatism in relation to phylogeny and ecology. Annu. Rev. Ecol. Evol. Syst. 34, 27–49 (2003)

    Article  Google Scholar 

  20. Hadfield, J. D. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010)

    Article  Google Scholar 

  21. von Hardenberg, A. & Gonzalez-Voyer, A. Disentangling evolutionary cause-effect relationships with phylogenetic confirmatory path analysis. Evolution 67, 378–387 (2013)

    PubMed  Article  Google Scholar 

  22. 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)

    Article  Google Scholar 

  23. Ricklefs, R. E. Insights from comparative analyses of aging in birds and mammals. Aging Cell 9, 273–284 (2010)

    CAS  PubMed  Article  Google Scholar 

  24. Stutchbury, B. J. & Morton, E. S. Behavioral Ecology of Tropical Birds (Academic, 2001)

  25. Bailey, S. F. Latitudinal gradients in colors and patterns of passerine birds. Condor 80, 372–381 (1978)

    Article  Google Scholar 

  26. 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)

    CAS  PubMed  Article  Google Scholar 

  27. Irwin, R. E. The evolution of plumage dichromatism in the New World blackbirds: social selection on female brightness. Am. Nat. 144, 890–907 (1994)

    Article  Google Scholar 

  28. 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)

    PubMed  Article  PubMed Central  Google Scholar 

  29. Emlen, S. T. & Oring, L. W. Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223 (1977)

    CAS  PubMed  Google Scholar 

  30. 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)

    ADS  CAS  Article  PubMed  Google Scholar 

  31. Valcu, M. & Dale, J. colorZapper: color extraction utilities. R package version 1.0. https://github.com/valcu/colorZapper (2014)

  32. Craig, A. in Handbook of the Birds of the World Vol. 15 (eds Del Hoyo, J., Elliot, A. & Christie, D. A. ) (Lynx Edicions, 2010)

  33. Starck, J. M. Review of Handbook of the Birds of the World. Ethology 102, 436–440 (1996)

    Google Scholar 

  34. 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)

    Article  Google Scholar 

  35. Gray, D. A. Carotenoids and sexual dichromatism in North American passerine birds. Am. Nat. 148, 453–480 (1996)

    Article  Google Scholar 

  36. 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)

    Article  Google Scholar 

  37. 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)

    CAS  PubMed  Article  Google Scholar 

  38. 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)

    CAS  PubMed  Article  Google Scholar 

  39. 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)

    Article  Google Scholar 

  40. Cuthill, I. C. in Bird Colouration, Volume 1: Mechanisms and Measurements (eds Hill, G. E. & McGraw, K. J. ) 3–40 (Harvard Univ. Press, 2006)

  41. Dale, J. et al. Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism. Proc. R. Soc. B 274, 2971–2979 (2007)

    PubMed  Article  PubMed Central  Google Scholar 

  42. Calder, W. A. Size, Function, and Life History (Courier Corporation, 1996)

  43. Pianka, E. R. On r- and K-selection. Am. Nat. 104, 592–597 (1970)

    Article  Google Scholar 

  44. 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)

    Article  Google Scholar 

  45. 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)

    PubMed  Article  Google Scholar 

  46. 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)

    PubMed  Article  Google Scholar 

  47. 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)

    PubMed  PubMed Central  Article  Google Scholar 

  48. 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)

  49. Rubenstein, D. R. Sexual and social competition: broadening perspectives by defining female roles. Phil. Trans. R. Soc. B. 367, 2248–2252 (2012)

    PubMed  Article  PubMed Central  Google Scholar 

  50. Alerstam, T., Hedenström, A. & Åkesson, S. Long-distance migration: evolution and determinants. Oikos 103, 247–260 (2003)

    Article  Google Scholar 

  51. 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)

    PubMed  Article  PubMed Central  Google Scholar 

  52. 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)

    ADS  Article  Google Scholar 

  53. Dunning, J. B. CRC Handbook of Avian Body Masses 2nd edn (CRC, 2008)

  54. 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)

    Google Scholar 

  55. Land Processes Distributed Active Archive Center (LP DAAC). MODIS/Terra Land Surface Temperature/Emissivity 8-Day L3 Global 0.05Deg (LP DAAC, 2014)

  56. Marchant, S. & Higgins, P. J. Handbook of Australian, New Zealand & Antarctic Birds (Oxford Univ. Press, 1990–2006)

  57. 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)

  58. Brown, L. H., Urban, E. K. & Newmann, K. The Birds of Africa (Academic, 1982–2004)

  59. Hockey, P. A. R., Dean, W. R. J. & Ryan, P. G. Roberts — Birds of Southern Africa 7th edn (John Voelcker Bird Book Fund, 2005)

  60. Poole, A. & Gill, F. Birds of North America (Cornell Lab of Ornithology, 1992–2003)

  61. 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)

    CAS  PubMed  Article  Google Scholar 

  62. 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)

    CAS  PubMed  Article  Google Scholar 

  63. Cockburn, A. Prevalence of different modes of parental care in birds. Proc. R. Soc. B 273, 1375–1383 (2006)

    PubMed  Article  PubMed Central  Google Scholar 

  64. 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)

    Article  Google Scholar 

  65. 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)

    CAS  Article  PubMed  Google Scholar 

  66. Pagel, M. Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999)

    ADS  CAS  Article  PubMed  Google Scholar 

  67. Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008)

    ADS  CAS  PubMed  Article  Google Scholar 

  68. 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)

    PubMed  Article  Google Scholar 

  69. Paradis, E., Claude, J. & Strimmer, K. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004)

    CAS  PubMed  Article  Google Scholar 

  70. 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)

  71. Revell, L. J. Phylogenetic signal and linear regression on species data. Methods Ecol. Evol. 1, 319–329 (2010)

    Article  Google Scholar 

  72. Revell, L. J. Size-correction and principal components for interspecific comparative studies. Evolution 63, 3258–3268 (2009)

    PubMed  Article  Google Scholar 

  73. Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012)

    Google Scholar 

  74. R Core Team. R: A language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2014)

  75. Schielzeth, H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1, 103–113 (2010)

    Article  Google Scholar 

  76. 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)

    MathSciNet  PubMed  MATH  Article  ADS  Google Scholar 

  77. 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)

    PubMed  Article  Google Scholar 

  78. Hansen, T. F. in Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (ed. Garamszegi, L. Z. ) 351–379 (Springer, 2014)

  79. 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)

  80. Shipley, B. A new inferential test for path models based on directed acyclic graphs. Struct. Equ. Modeling 7, 206–218 (2000)

    MathSciNet  Article  Google Scholar 

  81. Shipley, B. Cause and Correlation in Biology: a User’s Guide to Path Analysis, Structural Equations and Causal Inference (Cambridge Univ. Press, 2002)

  82. 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)

  83. Shipley, B. The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology 94, 560–564 (2013)

    PubMed  Article  Google Scholar 

  84. Arnold, T. W. Uninformative parameters and model selection using Akaike’s information criterion. J. Wildl. Mgmt. 74, 1175–1178 (2010)

    Article  Google Scholar 

  85. Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002)

Download references

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.

Author information

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.

Ethics declarations

Competing interests

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

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature15509

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing