Abstract

How populations diverge into different lineages is a central issue in evolutionary biology. Despite the increasing evidence indicating that such divergences do not need geographic isolation, numerous phenotypic differentiations show a distributional correspondence. In addition, gene flow has been widely detected during and through such diverging processes. We used one widely distributed Aquilegia viridiflora complex as a model system to examine genomic differentiation and corresponding phenotypic variations along geographic gradients. Our phenotypic analyses of 90 individuals from 20 populations from northwest to northeast China identified two phenotypic groups along the geographic cline. All examined traits are distinct between them although a few intermediate individuals occur in their contacting regions. We further sequenced the genomes of the representative individuals of each population. However, we recovered four distinct genetic lineages based on both nuclear genomes and plastomes that were different from phenotypic differentiation. In particular, we recovered numerous genetic hybrids in the contact regions of four lineages. Gene flow is widespread and continuous between four lineages but much higher between contacting lineages than geographically isolated lineages. In addition, many genes with fast lineage-specific mutations were identified to be involved in local adaptation. Our results suggest that both geographic isolation and local selection exerted by the environment may together create geographic distributions of phenotypic variations as well as the underlying genomic divergences in numerous lineages.