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The pace of tree microevolution during Anthropocene warming is largely unknown. We used a retrospective approach to monitor genomic changes in oak trees since the Little Ice Age (LIA). Allelic frequency changes were assessed from whole-genome pooled sequences for four age-structured cohorts of sessile oak (Quercus petraea) dating back to 1680, in each of three different oak forests in France. The genetic covariances of allelic frequency changes increased between successive time periods, highlighting genome-wide effects of linked selection. We found imprints of parallel linked selection in the three forests during the late LIA, and a shift of selection during more recent time periods of the Anthropocene. The changes in allelic covariances within and between forests mirrored the documented changes in the occurrence of extreme events (droughts and frosts) over the last 300 years. The genomic regions with the highest covariances were enriched in genes involved in plant responses to pathogens and abiotic stresses (temperature and drought). These responses are consistent with the reported sequence of frost (or drought) and disease damage ultimately leading to the oak dieback after extreme events. They provide support for adaptive evolution of long-lived species during recent climatic changes. Although we acknowledge that other sources (e.g., gene flow, generation overlap) may have contributed to temporal covariances of allelic frequency changes, the consistent and correlated response across the three forests lends support to the existence of a systematic driving force such as natural selection.

Oaks are an important part of our natural and cultural heritage. Not only are they ubiquitous in our most common landscapes' but they have also supplied human societies with invaluable services, including food and shelter, since prehistoric times(2). With 450 species spread throughout Asia, Europe and America(3), oaks constitute a critical global renewable resource. The longevity of oaks (several hundred years) probably underlies their emblematic cultural and historical importance. Such long-lived sessile organisms must persist in the face of a wide range of abiotic and biotic threats over their lifespans. We investigated the genomic features associated with such a long lifespan by sequencing, assembling and annotating the oak genome. We then used the growing number of whole-genome sequences for plants (including tree and herbaceous species) to investigate the parallel evolution of genomic characteristics potentially underpinning tree longevity. A further consequence of the long lifespan of trees is their accumulation of somatic mutations during mitotic divisions of stem cells present in the shoot apical meristems. Empirical(4) and modelling(5) approaches have shown that intra-organismal genetic heterogeneity can be selected for(6) and provides direct fitness benefits in the arms race with short-lived pests and pathogens through a patchwork of intra-organismal phenotypes(7). However, there is no clear proof that large-statured trees consist of a genetic mosaic of clonally distinct cell lineages within and between branches. Through this case study of oak, we demonstrate the accumulation and transmission of somatic mutations and the expansion of disease-resistance gene families in trees.