ABSTRACT
A fundamental goal in evolutionary biology is to understand the genetic architecture of adaptive traits. Using whole-genome data of 3955 of Darwin's finches on the Galápagos Island of Daphne Major, we identified six loci of large effect that explain 45% of the variation in the highly heritable beak size of Geospiza fortis, a key ecological trait. The major locus is a supergene comprising four genes. Abrupt changes in allele frequencies at the loci accompanied a strong change in beak size caused by natural selection during a drought. A gradual change in Geospiza scandens occurred across 30 years as a result of introgressive hybridization with G. fortis. This study shows how a few loci with large effect on a fitness-related trait contribute to the genetic potential for rapid adaptive radiation.
Subject(s)
Adaptation, Biological , Beak , Finches , Genetic Introgression , Genetic Speciation , Selection, Genetic , Animals , Beak/anatomy & histology , Ecuador , Finches/anatomy & histology , Finches/genetics , Gene Frequency , Metagenomics , Genetic LociABSTRACT
Carotenoid-based polymorphisms are widespread in populations of birds, fish, and reptiles,1 but generally little is known about the factors affecting their maintenance in populations.2 We report a combined field and molecular-genetic investigation of a nestling beak color polymorphism in Darwin's finches. Beaks are pink or yellow, and yellow is recessive.3 Here we show that the polymorphism arose in the Galápagos half a million years ago through a mutation associated with regulatory change in the BCO2 gene and is shared by 14 descendant species. The polymorphism is probably a balanced polymorphism, maintained by ecological selection associated with survival and diet. In cactus finches, the frequency of the yellow genotype is correlated with cactus fruit abundance and greater hatching success and may be altered by introgressive hybridization. Polymorphisms that are hidden as adults, as here, may be far more common than is currently recognized, and contribute to diversification in ways that are yet to be discovered.