Effects of mutations in pigeonMc1rimplicate an expanded plumage color patterning regulatory network

Abstract

AbstractStudies in mammals have shown that the Melanocortin 1 receptor occupies a pivotal role as a nexus for integrating paracrine and autocrine signals to regulate pigment production and type-switching between pheomelanin (red/yellow) and eumelanin (black/brown) pigment synthesis in melanocytes. Inactivating mutations in theMc1rgene are responsible for recessive pheomelanic reddening traits in several species, while mutations that increase activity cause dominant eumelanic darkening traits in mammals and birds. Previous efforts to associateMc1rcoding variants with color variation in pigeons (Columba livia) have yielded conflicting results. Applying a reverse genomic approach, we discovered a novel 500 base pair frameshifting deletion in pigeonMc1rthat likely inactivates the single-exon gene. Segregation analysis revealed complete cosegregation (LOD = 12.2) withsmoky(symbolsy), a recessive pigmentation trait reported in these pages by Willard F. Hollander 80 years ago. We coupled these findings with breeding tests to determine thatDirty(V), a dominant darkening trait, is allelic tosy, and identified two independentValleles, one of which is associated with melanic morphs of two other bird species. In contrast to observations thatMc1rinactivation results in uniform pheomelanic pelage in mammals, its loss in otherwise wild-type pigeons occurs without apparent pheomelanism, instead increasing plumage eumelanism while leaving black bar pattern elements of the tail and wing largely intact. These findings require reconsideration of Mc1r’s presumed role in pigment type-switching in birds, and suggest the existence of Mc1r-independent pathways for eumelanic pigmentation pattern regulation unknown in mammals.