A supergene and genomic mosaicism are associated with phenotypic evolution in Galápagos tree finches

Abstract Adaptive radiations provide powerful models to study the origins of phenotypic novelty and species diversity. Darwin’s finches constitute a classic example of adaptive radiation, in which beak morphology is a key trait related to fitness. Here, we focus on Camarhynchus tree finches by analyzing whole genomes in combination with morphological data to revisit long-standing questions regarding their origins raised before genetic evidence became available. Camarhynchus diversified over the last 100,000 years, yielding some striking morphological differences despite shallow genetic divergence. We identify several highly differentiated loci, including G03 , a supergene affecting beak and body size. We reveal a striking example of genomic mosaicism, in which autosomal differentiation between two sympatric species is restricted primarily to a single locus -( G03 )- that approaches fixation, shifting them from one phenotypic optimum to another. Contextualized in a broader phylogenetic framework, we also reveal an unexpected diversity of G03 haplotypes and show that the small and large G03 alleles diverged early in the radiation, suggesting a key genetic innovation enabling ecological expansion among species of Darwin’s finches. Our results further establish Camarhynchus as a model example of speciation with gene flow, underscoring the broader role of hybridization in generating biodiversity.