Secondary contacts between European white oaks reveal genes underlying reproductive isolation

Oaks are dominant forest tree species widely distributed across the Northern hemisphere, where they constitute natural resources of economical, ecological, social and historical value. Hybridization and adaptive introgression has long been advocated as a major evolutionary driver of their ecological success. Yet, a key question of their diversification in the context of interspecific gene flow is the maintenance of species barriers. Here, we developed a demographically-explicit genome scan approach combining Approximate Bayesian Computation and backward simulations to scan genomes of four European white oak species for reproductive barriers. We first confirmed earlier findings highlighting interspecific contacts occurring after the last glacial maximum. We then took advantage of the huge genetic variation observed between these four species (31 106 SNPs) to identify genomic regions mostly enriched in SNPs deviating from demographic expectations under recent secondary contacts. Detected outlier-enriched regions were restricted in size, widely distributed over all chromosomes. Our scan detected 215 regions containing 227 oak genes. Literature-based functional annotation of the underlying genes highlighted important functions driving reproductive isolation between the four species. These included genes involved in tolerance to biotic and abiotic constraints, and in intrinsic mating barriers. The functions of the annotated genes fit well with the ecological preferences of the four species. Hence these genes may be considered as candidates to investigate species responses to past and ongoing environmental changes.