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Whole genome characterizations of crop plants based on ancient DNA have provided unique keys for a better understanding of the evolutionary origins of modern cultivars, the pace and mode of selection underlying their adaptation to new environments and the production of phenotypes of interest. Although forests are among the most biologically rich ecosystems on earth and represent a fundamental resource for human societies, no ancient genome sequences have been generated for trees. This contrasts with the generation of multiple ancient reference genomes for important crops. Here, we sequenced the first ancient tree genomes using two white oak wood remains from Germany dating to the Last Little Ice Age (15th century CE, 7.3× and 4.0×) and one from France dating to the Bronze Age (1700 BCE, 3.4×). We assessed the underlying species and identified one medieval remains as a hybrid between two common oak species (Quercus robur and Q. petraea) and the other two remains as Q. robur. We found that diversity at the global genome level had not changed over time. However, exploratory analyses suggested that a reduction of diversity took place at different time periods. Finally, we determined the timing of leaf unfolding for ancient trees for the first time. The study extends the application of ancient wood beyond the classical proxies of dendroclimatology, dendrochronology, dendroarchaeology and dendroecology, thereby enhancing resolution of inferences on the responses of forest ecosystems to past environmental changes, epidemics and silvicultural practices. see also the Perspective by Andrew L. Hipp and Desanka Lazic [ABSTRACT FROM AUTHOR]

Summary: Oaks are dominant forest tree species widely distributed across the Northern Hemisphere, where they constitute natural resources of economic, ecological, social and historical value. Hybridisation and adaptive introgression have long been thought to be major drivers of their ecological success. Therefore, the maintenance of species barriers remains a key question, given the extent of interspecific gene flow.In this study, we made use of the tremendous genetic variation among four European white oak species (31 million single nucleotide polymorphisms (SNPs)) to infer the evolutionary history of these species, study patterns of genetic differentiation and identify reproductive barriers.We first analysed the ecological and historical relationships among these species and inferred a long‐term strict isolation followed by a recent and extensive postglacial contact using approximate Bayesian computation. Assuming this demographic scenario, we then performed backward simulations to generate the expected distributions of differentiation under neutrality to scan their genomes for reproductive barriers. We finally identified important intrinsic and ecological functions driving the reproductive isolation.We discussed the importance of identifying the genetic basis for the ecological preferences between these oak species and its implications for the renewal of European forests under global warming. See also the Editorial on this article by Plomion & Martin, 226: 943–946. [ABSTRACT FROM AUTHOR]

Summary: Latitudinal and elevational gradients provide valuable experimental settings for studies of the potential impact of global warming on forest tree species. The availability of long‐term phenological surveys in common garden experiments for traits associated with climate, such as bud flushing for sessile oaks (Quercus petraea), provide an ideal opportunity to investigate this impact.We sequenced 18 sessile oak populations and used available sequencing data for three other closely related European white oak species (Quercus pyrenaica, Quercus pubescens, and Quercus robur) to explore the evolutionary processes responsible for shaping the genetic variation across latitudinal and elevational gradients in extant sessile oaks. We used phenotypic surveys in common garden experiments and climatic data for the population of origin to perform genome‐wide scans for population differentiation and genotype–environment and genotype–phenotype associations.The inferred historical relationships between Q. petraea populations suggest that interspecific gene flow occurred between Q. robur and Q. petraea populations from cooler or wetter areas. A genome‐wide scan of differentiation between Q. petraea populations identified single nucleotide polymorphisms (SNPs) displaying strong interspecific relative divergence between these two species. These SNPs followed genetic clines along climatic or phenotypic gradients, providing further support for the likely contribution of introgression to the adaptive divergence of Q. petraea populations.Overall, the results indicate that outliers and associated SNPs are Q. robur ancestry‐informative. We discuss the results of this study in the framework of the postglacial colonization scenario, in which introgression and diversifying selection have been proposed as essential drivers of Q. petraea microevolution. See also the Editorial on this article by Plomion & Martin, 226: 943–946. [ABSTRACT FROM AUTHOR]

Historical trajectories of tree species during the late Quaternary have been well reconstructed through genetic and palaeobotanical studies. However, many congeneric tree species are interfertile, and the timing and contribution of introgression to species divergence during their evolutionary history remains largely unknown., We quantified past and current gene flow events between four morphologically divergent oak species ( Quercus petraea, Q. robur, Q. pyrenaica, Q. pubescens), by two independent inference methods: diffusion approximation to the joint frequency spectrum (∂a∂i) and approximate Bayesian computation ( ABC). For each pair of species, alternative scenarios of speciation allowing gene flow over different timescales were evaluated., Analyses of 3524 single nucleotide polymorphisms ( SNPs) randomly distributed in the genome, showed that these species evolved in complete isolation for most of their history, but recently came into secondary contact, probably facilitated by the most recent period of postglacial warming., We demonstrated that: there was sufficient genetic differentiation before secondary contact for the accumulation of barriers to gene flow; and current European white oak genomes are a mosaic of genes that have crossed species boundaries and genes impermeable to gene flow. [ABSTRACT FROM AUTHOR]