Abstract
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.
This is a preview of subscription content, access via your institution
Relevant articles
Open Access articles citing this article.
-
Molecular taxonomical identification and phylogenetic relationships of some marine dominant algal species during red tide and harmful algal blooms along Egyptian coasts in the Alexandria region
Environmental Science and Pollution Research Open Access 14 March 2022
-
Rapid phenotypic change in a polymorphic salamander over 43 years
Scientific Reports Open Access 22 November 2021
-
Accelerated diversifications in three diverse families of morphologically complex lichen-forming fungi link to major historical events
Scientific Reports Open Access 28 June 2019
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Rent or buy this article
Get just this article for as long as you need it
$39.95
Prices may be subject to local taxes which are calculated during checkout



References
Gray, S. M. & McKinnon, J. S. Linking color polymorphism maintenance and speciation. Trends Ecol. Evol. 22, 71–79 (2007)
Huxley, J. S. Morphism in birds. Acta 6th Int. Ornithol. Cong. 309–328. (1954)
West-Eberhard, M. J. Alternative adaptations, speciation and phylogeny (a review). Proc. Natl Acad. Sci. USA 83, 1388–1392 (1986)
Ford, E. B. Polymorphism. Biol. Rev. Camb. Philos. Soc. 20, 73–88 (1945)
Ford, E. B. Ecological Genetics (Chapman and Hall, 1964)
Huxley, J. S. Evolution: the Modern Synthesis 2nd edn (Allen & Unwin, 1963)
Cain, A. J. & Sheppard, P. M. Natural selection in Cepaea . Genetics 39, 89–116 (1954)
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, 581–610 (2006)
Sinervo, B. & Svensson, E. Correlational selection and the evolution of genomic architecture. Heredity 89, 329–338 (2002)
Chunco, A. J., McKinnon, J. S. & Servedio, M. R. Microhabitat variation and sexual selection can maintain male color polymorphisms. Evolution 61, 2504–2515 (2007)
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, 435–443 (2001)
Otto, S. P., Servedio, M. R. & Nuismer, S. L. Frequency-dependent selection and the evolution of assortative mating. Genetics 179, 2091–2112 (2008)
Coyne, J. A. & Orr, A. H. Speciation (Sinauer Associates, 2004)
Herder, F., Pfaender, J. & Schliewen, U. K. Adaptive sympatric speciation of polychromatic “roundfin” sailfin silverside fish in Lake Matano (Sulawesi). Evolution 62, 2178–2195 (2008)
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, 1911–1918 (2003)
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, 367–378 (1999)
Forsman, A., Ahnesjo, J., Caesar, S. & Karlsson, M. A model of ecological and evolutionary consequences of color polymorphism. Ecology 89, 34–40 (2008)
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, 4254–4259 (2010)
McKinnon, J. S. & Pierotti, M. E. R. Colour polymorphism and correlated characters: genetic mechanisms and evolution. Mol. Ecol. 19, 5101–5125 (2010)
FitzJohn, R. G., Maddison, W. P. & Otto, S. P. Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58, 595–611 (2009)
Maddison, W. P., Midford, P. E. & Otto, S. P. Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56, 701–710 (2007)
de Queiroz, A. & Gatesy, J. The supermatrix approach to systematics. Trends Ecol. Evol. 22, 34–41 (2007)
Galeotti, P., Rubolini, D., Dunn, P. O. & Fasola, M. Colour polymorphism in birds: causes and functions. J. Evol. Biol. 16, 635–646 (2003)
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, 237–248 (2004)
Crespi, B. J. & Sandoval, C. P. Phylogenetic evidence for the evolution of ecological specialization in Timema walking-sticks. J. Evol. Biol. 13, 249–262 (2000)
Van Gossum, H. & Mattern, M. Y. A phylogenetic perspective on absence and presence of a sex-limited polymorphism. Anim. Biol. 58, 257–273 (2008)
Ricklefs, R. E. Estimating diversification rates from phylogenetic information. Trends Ecol. Evol. 22, 601–610 (2007)
Price, T. Speciation in Birds (Roberts and Co, 2008)
Endler, J. A. Geographic Variation, Speciation and Clines (Princeton Univ. Press, 1977)
Roulin, A. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol. Rev. Camb. Philos. Soc. 79, 815–848 (2004)
Hackett, S. J. et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008)
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, 130–145 (2009)
Sanderson, M. J., McMahon, M. M. & Steel, M. Phylogenomics with incomplete taxon coverage: the limits to inference. BMC Evol. Biol. 10, 155 (2010)
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, 77–82 (1994)
Rabosky, D. L. Extinction rates should not be estimated from molecular phylogenies. Evolution 64, 1816–1824 (2010)
Acknowledgements
We thank M. Elgar, J. Endler, L. Joseph, A. Moussalli, A. Phillimore, S. Pryke and D. Rabosky for critical comments. This work was supported by the Australian Research Council (DP1092908).
Author information
Authors and Affiliations
Contributions
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.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
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. (PDF 2438 kb)
Supplementary Data
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. (PDF 3369 kb)
Rights and permissions
About this article
Cite this article
Hugall, A., Stuart-Fox, D. Accelerated speciation in colour-polymorphic birds. Nature 485, 631–634 (2012). https://doi.org/10.1038/nature11050
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nature11050
This article is cited by
-
Facial color diversity of Polistes paper wasps
Insectes Sociaux (2023)
-
Molecular taxonomical identification and phylogenetic relationships of some marine dominant algal species during red tide and harmful algal blooms along Egyptian coasts in the Alexandria region
Environmental Science and Pollution Research (2022)
-
Rapid phenotypic change in a polymorphic salamander over 43 years
Scientific Reports (2021)
-
Parallel evolution of morphological traits and body shape in littoral and pelagic brook charr, Salvelinus fontinalis, along a gradient of interspecific competition
Oecologia (2021)
-
Negative assortative mating and maintenance of shell colour polymorphism in Littorina (Neritrema) species
Marine Biology (2021)
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.