Intercontinental genomic parallelism in multiple adaptive radiations

Abstract

Parallelism, the evolution of similar traits in populations diversifying in similar conditions, provides good evidence of adaptation by natural selection. Many studies of parallelism have focused on comparisons of strongly different ecotypes or sharply contrasting environments, defined a priori, which could upwardly bias the apparent prevalence of parallelism. Here, we estimated genomic parallelism associated with individual components of environmental and phenotypic variation at an intercontinental scale across four adaptive radiations of the three-spined stickleback (Gasterosteus aculeatus), by associating genome-wide allele frequencies with continuous distributions of environmental and phenotypic variation. We found that genomic parallelism was well predicted by parallelism of phenotype-environment associations, suggesting that a quantitative characterization of phenotypes and environments can provide a good prediction of expected genomic parallelism. Further, we examined the explanatory power of genetic, phenotypic, and environmental similarity in predicting parallelism. We found that parallelism tended to be greater for geographically proximate, genetically similar radiations, highlighting the significant contingency of standing variation in the early stages of adaptive radiations, before new mutations accumulate. However, we also demonstrate that distance within multivariate environmental space predicts parallelism, after correction for genetic distance. This study thus demonstrates the relative influences of environment, phenotype and genetic contingency on repeatable signatures of adaptation in the genome.