Testing whether macroevolution follows microevolution: Are colour differences among swans (Cygnus) attributable to variation at the MC1R locus?

Abstract

BackgroundThe MC1R (melanocortin-1 receptor) locus underlies intraspecific variation in melanin-based dark plumage coloration in several unrelated birds with plumage polymorphisms. There is far less evidence for functional variants of MC1R being involved in interspecific variation, in which spurious genotype-phenotype associations arising through population history are a far greater problem than in intraspecific studies. We investigated the relationship between MC1R variation and plumage coloration in swans (Cygnus), which show extreme variation in melanic plumage phenotypes among species (white to black).ResultsThe two species with melanic plumage, C. atratus and C. melanocoryphus (black and black-necked swans respectively), both have amino acid changes at important functional sites in MC1R that are consistent with increased MC1R activity and melanism. Reconstruction of MC1R evolution over a newly generated independent molecular phylogeny of Cygnus and related genera shows that these putative melanizing mutations were independently derived in the two melanic lineages. However, interpretation is complicated by the fact that one of the outgroup genera, Coscoroba, also has a putative melanizing mutation at MC1R that has arisen independently but has nearly pure white plumage. Epistasis at other loci seems the most likely explanation for this discrepancy. Unexpectedly, the phylogeny shows that the genus Cygnus may not be monophyletic, with C. melanocoryphus placed as a sister group to true geese (Anser), but further data will be needed to confirm this.ConclusionOur study highlights the difficulty of extrapolating from intraspecific studies to understand the genetic basis of interspecific adaptive phenotypic evolution, even with a gene whose structure-function relationships are as well understood as MC1R as confounding variation make clear genotype/phenotype associations difficult at the macroevolutionary scale. However, the identification of substitutions in the black and black-necked swan that are known to be associated with melanic phenotypes, suggests Cygnus may be another example where there appears to be convergent evolution at MC1R. This study therefore provides a novel example where previously described intraspecific genotype/phenotype associations occur at the macroevolutionary level.