Pervasive historical introgression across oak phylogeny shapes gene expression

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Abstract Oaks have been called the “worst-case scenario” for the biological species concept because of the presumed importance of introgression among species. However, we still lack an estimation of the importance of genome-wide introgression across the eight sections of the Quercus phylogeny. Nor do we have a complete characterization of what is introgressed and how it functionally influences the recipient species. Firstly, we used 168 whole genomes from 67 Quercus species belonging to the eight sections of the Quercus phylogeny and a super pan-genome based on 9 species to generate a phylogeny and test for incomplete lineage sorting and hybridization. Introgression was widespread and occurred within and across the eight sections. Ancient introgression occurred between sections, while more recent introgression took place within sections. Secondly, using genome-wide transcriptome and methylome from a subset of 19 species sampled from four sections we demonstrated that introgressed genes tend to be more highly and uniformly expressed than non-introgressed ones. This difference in expression level between introgressed and non-introgressed genes mostly results from cis-regulation, and both methylation and chromatin accessibility explain the high and conserved expression of introgressed genes across species. In summary, introgression has been a major evolutionary force during the whole evolutionary history of Quercus and had a significant impact on fundamental processes such as gene regulation and expression. Significance Statement Many oak species have been known to exchange genes during their evolution. However, there are more than 400 oak species today, divided into eight phylogenetic sections and distributed over four continents, and the extent to which introgression has affected the whole oak phylogeny remains unknown. Using whole genomes from 67 oak species belonging to the eight sections we show that introgression occurred within and across the eight sections. Ancient introgression occurred between sections, but more recent introgression took place within section. Using genome-wide gene expression and methylation data from a subset of species we also demonstrated that introgression affected gene regulation and expression: introgressed genes are more highly and uniformly expressed than non-introgressed ones.

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