Genetic and epigenetic signatures associated with the rapid radiation of Aquilegia species

Elucidating how the diverse evolutionary mechanisms interact to determine species diversification is crucial to understanding the evolution and persistence of biodiversity. The genus Aquilegia (columbine) is a model system to identify genetic and epigenetic signatures underpinning the rapid adaptive radiation. In this study, we surveyed the genomes and DNA methylomes of ten worldwide Aquilegia species to investigate whether specific genomic architectures were associated with rapid species diversification in the Asian, European and North American lineages. The resulting phylogenies and population structure inferences revealed clearly high genetic and DNA methylomic divergence among the three lineages. Genome-wide scanning demonstrated significantly higher positive and purifying selection pressures among the Asian species compared to the European and North American lineages. More importantly, candidate genes identified at the genetic and epigenetic levels are functionally related to diverse adaptation-related traits, such as stress tolerance, photosynthesis and cell reproduction. While a considerable proportion of the candidate genes share hotspots of intra- and inter-lineage divergence, genetic and epigenetic factors were found to act on complementary biological pathways. By assessing the interaction between genetic variations and epigenetic variability, we found that epigenetic variability is a partially independent factor that intertwines with genetic mechanism to facilitate the diversification of the Aquilegia species. Taken together, these findings suggest that specific genetic architectures have been involved in vital biological pathways in response to diverse environmental conditions and epigenetic modifications may play a complementary role in the process of adaptive speciation. Our study provides an exploratory overview of how the established genetic and epigenetic signatures are associated with the rapid species diversification of Aquilegia species.