The evolution of black plumage from blue in Australian fairy‐wrens (Maluridae): genetic and structural evidence

Abstract

Genetic variation in the melanocortin‐1 receptor (MC1R) locus is responsible for color variation, particularly melanism, in many groups of vertebrates. Fairy‐wrens, Maluridae, are a family of Australian and New Guinean passerines with several instances of dramatic shifts in plumage coloration, both intra‐ and inter‐specifically. A number of these color changes are from bright blue to black plumage. In this study, we examined sequence variation at the MC1R locus in most genera and species of fairy‐wrens. Our primary focus was subspecies of the white‐winged fairy‐wren Malurus leucopterus in which two subspecies, each endemic to islands off the western Australian coast, are black while the mainland subspecies is blue. We found fourteen variable amino acid residues within M. leucopterus, but at only one position were alleles perfectly correlated with plumage color. Comparison with other fairy‐wren species showed that the blue mainland subspecies, not the black island subspecies, had a unique genotype. Examination of MC1R protein sequence variation across our sample of fairy‐wrens revealed no correlation between plumage color and sequence in this group. We thus conclude that amino acid changes in the MC1R locus are not directly responsible for the black plumage of the island subspecies of M. leucopterus. Our examination of the nanostructure of feathers from both black and blue subspecies of M. leucopterus and other black and blue fairy‐wren species clarifies the evolution of black plumage in this family. Our data indicate that the black white‐winged fairy‐wrens evolved from blue ancestors because vestiges of the nanostructure required for the production of blue coloration exist within their black feathers. Based on our phylogeographic analysis of M. leucopterus, in which the two black subspecies do not appear to be each other's closest relatives, we infer that there have been two independent evolutionary transitions from blue to black plumage. A third potential transition from blue to black appears to have occurred in a sister clade.