Community-wide genome sequencing reveals 30 years of Darwin’s finch evolution

Abstract

INTRODUCTION: Adaptive radiations are groups of organisms that have diverged ecologically from a common ancestor relatively rapidly. They have yielded important insights into the ecology, behavior, and genetics of speciation through inferences of the evolutionary processes that most likely gave rise to observed patterns of divergence. In a few cases, experiments have substantiated these inferences by testing hypotheses of causal mechanisms. Our understanding of evolutionary radiations has been transformed in the past decade by discoveries of the genomic variation underlying phenotypic divergence. The dynamic genomic variation responsible for rapid evolutionary change in contemporary populations in nature, and its connection with evolution in the past, is not well known. RATIONALE: We set out to establish the link between contemporary and past evolution in a well-studied system, Darwin’s finches in the Galápagos archipelago. Eighteen species have evolved from a common ancestor in the last million years. They diverged in beak morphology and body size, and to a small extent, in plumage. Two evolutionary processes, natural selection and introgressive hybridization, influenced the outcomes of phenotypic evolution in this adaptive radiation. We followed the fates of individually marked and measured birds of four Geospiza species on Daphne Major Island for 40 years to investigate contemporary evolution. We combined observations on fitness with whole-genome sequencing to reveal and interpret the genetic architecture of evolutionary change. RESULTS: We used whole-genome resequencing data to track evolutionary change in 3955 finches of four Geospiza species. We identified six loci that together explain as much as 45% of variation in beak size of G. fortis (medium ground finch), a highly heritable and key ecological trait. One locus alone is responsible for 25% of variation in beak size and 13% of variation in body size, and is most likely a supergene comprising four genes that contain multiple adaptive mutations with phenotypic consequences for both traits. The haplotypes associated with large and small beak size were established before the divergence of Geospiza ground finches and Camarynchus tree finches. Abrupt changes in allele frequencies at these loci in G. fortis resulted from strong natural selection during an extreme drought and explained a large part of the shift in beak size. Introgression of small-beak alleles from the smaller G. fuliginosa influenced the outcome of natural selection by increasing the frequency of small alleles in G. fortis. In the cactus-feeding G. scandens population, we observed more gradual changes in allele frequencies over the study period resulting from introgression. CONCLUSION: We show that a few loci of large effect have had a major impact on the trajectory of Darwin’s finch populations on the small island of Daphne Major. They affect fitness through their association with survival in relation to competition for food, particularly during extreme climatic events, and have been passed between species through hybridization. A reasonable explanation for the presence of large-effect alleles in Darwin’s finches is that these have evolved over time by the accumulation of multiple causal mutations as a response to diversifying selection. They contribute both to phenotypic differences between species and to phenotypic diversity within G. fortis. This genetic architecture differs from the one documented for many polygenic traits in other species lacking large-effect loci, such as beak morphology in some other birds and human stature, which is likely due to differences among species in selection regimes and the impact of gene exchange. These genetic changes at the population level reveal the dynamics of evolutionary change in this iconic adaptive radiation.