Concordant evolution of plumage colour, feather microstructure and a melanocortin receptor gene between mainland and island populations of a fairy–wren

Abstract

Studies of the patterns of diversification of birds on islands have contributed a great deal to the development of evolutionary theory. In white-winged fairy-wrens, Malurus leucopterus, mainland males develop a striking blue nuptial plumage whereas those on nearby islands develop black nuptial plumage. We explore the proximate basis for this divergence by combining microstructural feather analysis with an investigation of genetic variation at the melanocortin-1 receptor locus (MC1R). Fourier analysis revealed that the medullary keratin matrix (spongy layer) of the feather barbs of blue males was ordered at the appropriate nanoscale to produce the observed blue colour by coherent light scattering. Surprisingly, the feather barbs of black males also contained a spongy layer that could produce a similar blue colour. However, black males had more melanin in their barbs than blue males, and this melanin may effectively mask any structural colour produced by the spongy layer. Moreover, the presence of this spongy layer suggests that black island males evolved from a blue-plumaged ancestor. We also document concordant patterns of variation at the MC1R locus, as five amino acid substitutions were perfectly associated with the divergent blue and black plumage phenotypes. Thus, with the possible involvement of a melanocortin receptor locus, increased melanin density may mask the blue-producing microstructure in black island males, resulting in the divergence of plumage coloration between mainland and island white-winged fairy-wrens. Such mechanisms may also be responsible for plumage colour diversity across broader geographical and evolutionary scales.

A window on the genetics of evolution:MC1Rand plumage colouration in birds

“…Ultrastructural studies indicate that the melanic subspecies arose from an ancestor with blue males. However, comparison with an out-group shows that, unexpectedly, many MC1R substitutions have occurred in the lineage leading to the blue subspecies (Doucet et al 2004), so it will be important in this case to demonstrate that the differences at MC1R do not merely reflect population divergence.…”

“…An island subspecies of the white-winged fairy-wren (Malurus leucopterus) in which males in nuptial plumage are melanic shows strong differentiation at MC1R from a mainland subspecies in which males are blue (Doucet et al 2004). An interesting aspect of this example is that there is sexual dimorphism in melanism, and females are not melanic.…”

The Evolution of Signal Design in Manakin Plumage Ornaments

“…Structural colors can also be subdivided into two categories. Noniridescent structural colors are produced by coherently scattered light within a matrix of keratin and air spaces in feather barbs and generally produce blue, violet, and ultraviolet colors (Prum et al 1999(Prum et al , 2003Shawkey et al 2003;Doucet et al 2004). Iridescent structural colors are produced by coherently scattered light from stacked arrays of melanin granules within feather barbules and can produce iridescent hues spanning the bird-visible spectrum (Brink and van der Berg 2004;Doucet et al 2006;Prum 2006).…”

Age‐ and quality‐dependent DNA methylation correlate with melanin‐based coloration in a wild bird

“…To date, the majority of studies of melanin‐based traits have focused on the genes encoding the melanocortin system and characterized either genetic variation between species (Doucet, Shawkey, Rathburn, Mays, & Montgomerie, 2004; Toews et al., 2016) or how mutations in genes like the MC1R are associated with different melanin‐based phenotypes within species (Peters et al., 2016; San‐Jose et al., 2017). So far, only a single study has examined how DNA methylation may impact melanin coloration.…”