Mutations in different pigmentation genes are associated with parallel melanism in island flycatchers

Abstract

The independent evolution of similar traits across multiple taxa provides some of the most compelling evidence of natural selection. Little is known, however, about the genetic basis of these convergent or parallel traits: are they mediated by identical or different mutations in the same genes, or unique mutations in different genes? Using a combination of candidate gene and reduced representation genomic sequencing approaches, we explore the genetic basis of and the evolutionary processes that mediate similar plumage colour shared by isolated populations of the Monarcha castaneiventris flycatcher of the Solomon Islands. A genome-wide association study (GWAS) that explicitly controlled for population structure revealed that mutations in known pigmentation genes are the best predictors of parallel plumage colour. That is, entirely black or melanic birds from one small island share an amino acid substitution in the melanocortin-1 receptor (MC1R), whereas similarly melanic birds from another small island over 100 km away share an amino acid substitution in a predicted binding site of agouti signalling protein (ASIP). A third larger island, which separates the two melanic populations, is inhabited by birds with chestnut bellies that lack the melanic MC1R and ASIP allelic variants. Formal F ST outlier tests corroborated the results of the GWAS and suggested that strong, directional selection drives the near fixation of the MC1R and ASIP variants across islands. Our results, therefore, suggest that selection acting on different mutations with large phenotypic effects can drive the evolution of parallel melanism, despite the relatively small population size on islands.

Admixture mapping in a hybrid zone reveals loci associated with avian feather coloration

“…If true, this contrasts with the recessive inheritance pattern of black throat colour in goldenwinged warblers, which was predicted to be a recessive Mendelian trait [56] and recently confirmed with genomic data [18]. Other melanin-based traits in birds with known genetic basis are consistent with dominant [57] or partially dominant inheritance [14].…”

“…For instance, several studies have consistently identified coding changes as well as putative regulatory differences in the gene agouti signalling protein (ASIP) between birds with melanic and non-melanic plumage patches [1,14,18,28]. Our assay identified 72 SNPs within 50 kb of the ASIP coding region, but none were highly differentiated between myrtle and Audubon's warblers (average F ST in this region ¼ 0.02, lower than the genome-wide average of 0.045).…”

“…Much recent progress has been made identifying putative genes involved in generating coloration differences between related species [4,5,14,28,29,52]. In birds, coloration differences are derived primarily from two molecules-melanins and carotenoids-that have different biochemical processing [4,5].…”

“…In animals, this research has primarily focused on identifying the genes involved in the melanogenesis pathway, which produces melanin responsible for black or brown coloration [3,13,14]. However, in many species, particularly in birds, differences in red, orange and yellow coloration usually arise from variation in the distribution of carotenoid-derived pigments, the precursors of which cannot be synthesized endogenously and hence must be acquired from food [4].…”

The dark side of birds: melanism—facts and fiction

“…The eumelanistic morphs in different isolated populations of Chestnut-bellied Monarch Monarcha castaneiventris on the Solomon Islands are the result of two different mutations. The eumelanic plumage of birds on the small island of Santa Ana is the result of a variation of the MC1R, while equally black birds on two other small islands, Ugi and Three Sisters, possess a mutation of the agouti gene (Uy et al 2016).…”