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Genetic basis of the evolution of plumage coloration

Marie Pointer and Neil Walsh

There is very little known about the molecular genetic basis of the extraordinary diversity of plumage coloration in birds. The major pigments in birds are melanins (black, brown, rufous) and carotenoids (bright yellow, red). The pathways of melanin synthesis are evolutionarily conserved between birds and mammals, providing several candidate genes for involvement in evolution of melanin-based plumage differences.

Melanic polymorphisms have been extensively studied in some birds. One dramatic case of melanism is the bananaquit (Coereba flaveola), shown here. These nectarivorous passerines occur throughout the neotropics and the majority of populations consist of birds with a variable amount of bright yellow pigment on the breast. Completely black bananaquits occur on a few Caribbean islands. On Grenada and St. Vincent, the distribution of melanic bananaquits correlates with habitat: melanic birds occupy moist forest at varying altitude on these islands, in contrast to yellow-breasted birds which are only found in dry, disturbed lowland areas.

We investigated sequence variation in the melanocortin-1 receptor (MC1R) gene in melanic and yellow bananaquits and found a point mutation that is probably responsible for the coloration difference. Reconstruction of the history of melanism shows that, as expected, the melanic forms evolved from yellow birds (Theron et el. 2001).. Furthermore, we found that the MC1R also controls melanism in Lesser Snow Geese (Anser caerulescens caerulescens) and Arctic skuas (Stercorarius parasiticus) (Mundy et al. 2004). These are two classic examples of melanic polymorphism in which coloration has been shown to be important in mate choice. The results reveal a remarkable conservation in the genetic basis of melanism in avian evolution, and also shows that the MC1R can control quantitative variation in amounts and distribution of eumelanin (Mundy 2005). Recentlly, we found that MC1R variation may underly colour variation in swans (Pointer & Mundy 2008). However, MC1R is not involved in all cases of dramatic change in melanin content, as shown by a recent study on the carrion crow-hooded crow hybrid zone (Haas et al. 2009)..

Currently, we are following up these studies in a number of other cases of melanism in birds. We are also attempting to isolate genes underlying variation in the bright carotenoid-based colours of birds (widowbirds, bishops and queleas).

References

Haas, F., Pointer, M. A., Saino, N., Brodin, A., Mundy, N. I., and B. Hansson (2009) An analysis of population genetic differentiation and genotype–phenotype association across the hybrid zone of carrion and hooded crows using microsatellites and MC1R. Molecular Ecology 18, 294-305.

Pointer, M. A. and N. I. Mundy (2008) Testing whether macroevolution follows microevolution: Are colour differences among swans (Cygnus) attributable to variation at the MC1R locus? BMC Evolutionary Biology 8, 249.

Nadeau, N. J., Minvielle, F., Ito, S., Inoue-Murayama, M., Gourichon, D., Johns, S. A., Burke, T. and N. I. Mundy (2008) Characterization of Japanese quail yellow as a genomic deletion upstream of the avian homologue of the mammalian ASIP (agouti) gene. Genetics178, 777-786.

Nadeau, N. J., Burke, T. A. and N. I. Mundy (2007) Evolution of an avian pigmentation gene correlates with a measure of sexual selection. Proceedings of the Royal Society Series B 274, 1807-1813.

Nadeau, N. J., Mundy, N. I., Gourichon, D. and F. Minvielle (2007) Association of a single nucleotide substitution in TYRP1 with roux in Japanese quail (Coturnix japonica). Animal Genetics 38, 609-613

Mundy, N. I. (2006) The genetic basis of colour variation. In “Bird Coloration: Volume 1. Mechanisms and measurements”. pp469-506. Eds. G. E. Hill and K. McGraw. Harvard University Press.

Nadeau, N. J., Minvielle, F., and N. I. Mundy (2006) Association of a Glu92Lys substitution in MC1R with Extended brown in Japanese quail (Coturnix japonica). Animal Genetics 37, 287-289.

Mundy, N. I. (2005) A window on the genetics of evolution: MC1R and plumage coloration in birds. Proceedings of the Royal Society Series B 272, 1633-1640.

Mundy, N. I., Badcock, N., Hart, T., Scribner, K., Janssen, K. and N. J. Nadeau (2004) Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science 303, 1870-1873.

Mundy, N. I., Kelly, J., Theron, E. and K. Hawkins. (2003) Molecular evolutionary genetics of the melanocortin-1 receptor in vertebrates. Annals of the New York Academy of Sciences 994, 307-312.

Theron, E., Hawkins, K., Bermingham, E., Ricklefs, R. and N. I. Mundy. (2001) The molecular basis of an avian plumage polymorphism in the wild: a point mutation in the melanocortin-1 receptor is perfectly associated with melanism in the bananaquit (Coereba flaveola). Current Biology 11, 550-557.