Accelerated speciation in colour-polymorphic birds

Journal name:
Date published:
Published online

Colour polymorphism exemplifies extreme morphological diversity within populations1, 2. It is taxonomically widespread but generally rare. Theory suggests that where colour polymorphism does occur, processes generating and maintaining it can promote speciation but the generality of this claim is unclear1. Here we confirm, using species-level molecular phylogenies for five families of non-passerine birds, that colour polymorphism is associated with accelerated speciation rates in the three groups in which polymorphism is most prevalent. In all five groups, colour polymorphism is lost at a significantly greater rate than it is gained. Thus, the general rarity and phylogenetic dispersion of colour polymorphism is accounted for by a combination of higher speciation rate and higher transition rate from polymorphism to monomorphism, consistent with theoretical models where speciation is driven by fixation of one or more morphs3. This is corroborated by evidence from a species-level molecular phylogeny of passerines, incorporating 4,128 (66.5%) extant species, that polymorphic species tend to be younger than monomorphic species. Our results provide empirical support for the general proposition, dating from classical evolutionary theory2, 4, 5, 6, that colour polymorphism can increase speciation rates.

At a glance


  1. Speciation rate ([lgr]1/[lgr]0) ratio from Bayesian Diversitree analyses.
    Figure 1: Speciation rate (λ1/λ0) ratio from Bayesian Diversitree analyses.

    Values >1 indicate higher speciation rates for the colour-polymorphic state. *P0.05; **P0.01 for likelihood ratio tests (LRTs) comparing a model with two different speciation rates versus one with equal rates. Numbers on each bar are the colour-polymorphic taxa/total number of taxa (above) and sampling fractions for polymorphic/monomorphic species. Diversitree posterior distributions are shown with blueindicatingmonomorphic and redindicating polymorphic. Images are representative polymorphic species: grey goshawk, Accipiter novaehollandiae (photo: Á. Lumnitzer); eastern screech owl, Megascops asio (photo: J. Whitlock); Antillean nighthawk, Chordeiles gundlachii (photo: M. Landestoy); gyrfalcon, Falco rusticolus (; and ruffed grouse, Bonasa umbellus (photo: J. Pons).

  2. Ratio of transition rates (q10/q01) between states from Bayesian Diversitree analyses.
    Figure 2: Ratio of transition rates (q10/q01) between states from Bayesian Diversitree analyses.

    Values >1 indicate a higher transition rate from polymorphic to monomorphic than the converse. *P0.05; **P0.01 for LRTs comparing a model with two different transition rates versus one with equal rates. Diversitree posterior distributions of transition rates away from polymorphism are shown with blueindicatingmonomorphic and red indicating polymorphic. Images and credits as in Fig. 1.

  3. Randomization tests of relative tip branch lengths for passerine species.
    Figure 3: Randomization tests of relative tip branch lengths for passerine species.

    Mean difference between the tip branch length of 67 randomly chosen species and the median tip branch length for members of the relevant family. Lines show the distribution from 5,000 randomizations. Blue line shows all species and red line shows species belonging to polytypic genera (that is, excluding monotypic genera). Arrows indicate the observed value for colour-polymorphic species; both are in the left tail of the distribution, indicating that tip branch lengths of colour-polymorphic species tend to be shorter than monomorphic species. Dotted lines indicate 95% confidence intervals.


  1. Gray, S. M. & McKinnon, J. S. Linking color polymorphism maintenance and speciation. Trends Ecol. Evol. 22, 7179 (2007)
  2. Huxley, J. S. Morphism in birds. Acta 6th Int. Ornithol. Cong. 309328. (1954)
  3. West-Eberhard, M. J. Alternative adaptations, speciation and phylogeny (a review). Proc. Natl Acad. Sci. USA 83, 13881392 (1986)
  4. Ford, E. B. Polymorphism. Biol. Rev. Camb. Philos. Soc. 20, 7388 (1945)
  5. Ford, E. B. Ecological Genetics (Chapman and Hall, 1964)
  6. Huxley, J. S. Evolution: the Modern Synthesis 2nd edn (Allen & Unwin, 1963)
  7. Cain, A. J. & Sheppard, P. M. Natural selection in Cepaea. Genetics 39, 89116 (1954)
  8. Sinervo, B. & Calsbeek, R. The developmental, physiological, neural, and genetical causes and consequences of frequency-dependent selection in the wild. Annu. Rev. Ecol. Evol. Syst. 37, 581610 (2006)
  9. Sinervo, B. & Svensson, E. Correlational selection and the evolution of genomic architecture. Heredity 89, 329338 (2002)
  10. Chunco, A. J., McKinnon, J. S. & Servedio, M. R. Microhabitat variation and sexual selection can maintain male color polymorphisms. Evolution 61, 25042515 (2007)
  11. Lande, R., Seehausen, O. & van Alphen, J. J. M. Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish. Genetica 112–113, 435443 (2001)
  12. Otto, S. P., Servedio, M. R. & Nuismer, S. L. Frequency-dependent selection and the evolution of assortative mating. Genetics 179, 20912112 (2008)
  13. Coyne, J. A. & Orr, A. H. Speciation (Sinauer Associates, 2004)
  14. Herder, F., Pfaender, J. & Schliewen, U. K. Adaptive sympatric speciation of polychromatic “roundfin” sailfin silverside fish in Lake Matano (Sulawesi). Evolution 62, 21782195 (2008)
  15. Nosil, P., Crespi, B. J. & Sandoval, C. P. Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement. Proc. R. Soc. Lond. B 270, 19111918 (2003)
  16. Seehausen, O., van Alphen, J. J. M. & Lande, R. Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection. Ecol. Lett. 2, 367378 (1999)
  17. Forsman, A., Ahnesjo, J., Caesar, S. & Karlsson, M. A model of ecological and evolutionary consequences of color polymorphism. Ecology 89, 3440 (2008)
  18. Corl, A., Davis, A. R., Kuchta, S. R. & Sinervo, B. Selective loss of polymorphic mating types is associated with rapid phenotypic evolution during morphic speciation. Proc. Natl Acad. Sci. USA 107, 42544259 (2010)
  19. McKinnon, J. S. & Pierotti, M. E. R. Colour polymorphism and correlated characters: genetic mechanisms and evolution. Mol. Ecol. 19, 51015125 (2010)
  20. FitzJohn, R. G., Maddison, W. P. & Otto, S. P. Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58, 595611 (2009)
  21. Maddison, W. P., Midford, P. E. & Otto, S. P. Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56, 701710 (2007)
  22. de Queiroz, A. & Gatesy, J. The supermatrix approach to systematics. Trends Ecol. Evol. 22, 3441 (2007)
  23. Galeotti, P., Rubolini, D., Dunn, P. O. & Fasola, M. Colour polymorphism in birds: causes and functions. J. Evol. Biol. 16, 635646 (2003)
  24. Galeotti, P. & Rubolini, D. The niche variation hypothesis and the evolution of colour polymorphism in birds: a comparative study of owls, nightjars and raptors. Biol. J. Linn. Soc. 82, 237248 (2004)
  25. Crespi, B. J. & Sandoval, C. P. Phylogenetic evidence for the evolution of ecological specialization in Timema walking-sticks. J. Evol. Biol. 13, 249262 (2000)
  26. Van Gossum, H. & Mattern, M. Y. A phylogenetic perspective on absence and presence of a sex-limited polymorphism. Anim. Biol. 58, 257273 (2008)
  27. Ricklefs, R. E. Estimating diversification rates from phylogenetic information. Trends Ecol. Evol. 22, 601610 (2007)
  28. Price, T. Speciation in Birds (Roberts and Co, 2008)
  29. Endler, J. A. Geographic Variation, Speciation and Clines (Princeton Univ. Press, 1977)
  30. Roulin, A. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol. Rev. Camb. Philos. Soc. 79, 815848 (2004)
  31. Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 17631768 (2008)
  32. Lemmon, A. R., Brown, J. M., Stanger-Hall, K. & Lemmon, E. M. The effect of ambiguous data on phylogenetic estimates obtained by maximum likelihood and Bayesian inference. Syst. Biol. 58, 130145 (2009)
  33. Sanderson, M. J., McMahon, M. M. & Steel, M. Phylogenomics with incomplete taxon coverage: the limits to inference. BMC Evol. Biol. 10, 155 (2010)
  34. Nee, S., Holmes, E. C., May, R. M. & Harvey, P. H. Extinction rates can be estimated from molecular phylogenies. Philos. Trans. R. Soc. Lond. B 344, 7782 (1994)
  35. Rabosky, D. L. Extinction rates should not be estimated from molecular phylogenies. Evolution 64, 18161824 (2010)

Download references

Author information


  1. Department of Zoology, University of Melbourne, Melbourne, Victoria 3010, Australia

    • Andrew F. Hugall &
    • Devi Stuart-Fox
  2. Present address: Sciences Department, Melbourne Museum, Melbourne, Victoria 3053, Australia.

    • Andrew F. Hugall


A.F.H. constructed phylogenies, conducted diversification analyses, wrote the Methods, Supplementary Information and edited the main manuscript. D.S.-F. conceived and funded the project, wrote the main manuscript and edited remaining sections. Both authors contributed to interpretation of results.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

Author details

Supplementary information

PDF files

  1. Supplementary Information (2.3M)

    This file contains Supplementary Tables 1-7, Supplementary Figures 1-7, Supplementary Text and Supplementary Methods. Supplementary Tables 1 and 2 show sampling and summary statistics from diversification analyses; Supplementary Figure 1 and the Supplementary Text show the effects of sampling; and Supplementary Figure 1 also shows phylogenetic uncertainty. The Supplementary Methods contain detailed phylogenetic methods; Supplementary Tables S3-S7 and Supplementary Figure S2 contain summary statistics and additional information for phylogeny reconstruction; and Supplementary Figures S3-S7 contain phylogenies for the Accipitridae, Strigiformes, Caprimulgiformes, Falconidae and Galliformes.

  2. Supplementary Data (3.2M)

    This file contains newick format trees with node support values for the Strigiformes, Caprimulgiformes, Falconidae, Galliformes and four passerine trees: Lower Oscines-Corvoidea, Passeroidea, Suboscines; Genus-level tree.

Additional data