Understanding the relative roles of phenotypic plasticity and genetic differentiation in shaping plant phenological responses is essential for predicting forest tree responses to climate warming. Although spring and autumn phenophases respond sensitively to rising temperatures, the underlying regulatory mechanisms may differ substantially, particularly across environmental gradients. We investigated intra-specific phenological variation in Quercus petraea across the French Pyrenees using a multi-environment experimental framework. This approach integrated 15 years of in situ phenological monitoring with common garden (CG) and reciprocal transplant experiments spanning an elevational gradient. We quantified key phenological traits-leaf unfolding, leaf senescence, and growing season length-and applied generalized linear mixed models to evaluate the relative effects of temperature, provenance-level differentiation, and their interactions. Leaf unfolding showed strong temperature-associated plastic responses and comparatively limited provenance-level differentiation. In contrast, leaf senescence showed weaker and less consistent temperature responses. Growing season length increased under warmer conditions, largely reflecting the combined effects of earlier leaf unfolding and variable senescence timing. Our findings reveal phase-specific differences in phenological responses, with stronger temperature-associated plasticity in spring than in autumn phenology. These results highlight the need for long-term, multi-environmental data for understanding tree phenology under a changing climate and provide insights for developing adaptive forest management strategies that maintain adaptive capacity.

This review summarizes the contributions of genomics to our understanding of oak evolution and management, both past and ongoing. Far from being exhaustive given the large number of publications following the publication of the genomes, this review emphasizes work conducted in the decade following publication of the first two complete oak genome assemblies, and major findings and achievements regarding (1) oak evolutionary history, (2) speciation and introgression, and tools for (3) tree breeding and (4) management and conservation of native forests. While reviewing recent advances, the review also looks to the future by highlighting the research opportunities offered by genomics in conjunction with other developments in ecology and genetics.

Late spring frosts (LSF) have substantial ecological and economic impacts in the temperate and boreal zones. Yet, the effects of climate warming on the frequency (i.e., probability of LSF in a given year, in %) and extent (i.e., percentage of trees in a population damaged by a given LSF event) of LSF damage remain underexplored. Here, extending a budburst model that accounts for within-population variability, we developed and evaluated a new model of LSF damage occurrence and extent using 1,220 observations of LSF damage to newly emerged leaves from 304 oak populations in France (1997-2021). Our model simulations reveal that overall, French oak populations are, over time, less exposed to LSF amid ongoing climate change. We observed an overall decline in the frequency (-0.22 % per year) and extent (-0.34 % per year) of LSF damage in French oak populations over the past six decades (1961-2021). These trends are largely driven by the temporal advance of both the last spring frost day and budburst dates, with the last spring frost day advancing at a slightly faster rate (-0.28 days per year) than budburst (-0.21 days per year). This temporal mismatch explains why, contrary to the common assumption that earlier budburst increases frost risk, earlier budburst was in fact associated with a lower frequency of LSF damage. Nevertheless, considerable geographical variability emerged, with declines in damage frequency being more pronounced in continental regions, whereas declines in damage extent were more pronounced in coastal regions. Our findings underscore the importance of considering both LSF frequency and extent when assessing frost risks in a warming climate, offering a comprehensive framework for future ecological and economic evaluations of LSF impacts.

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.

Understanding genomic variation and adaptation of widespread tree species across their range is useful for predicting responses to environmental change and guiding sustainable forest management. Quercus rubra (Northern red oak) is a dominant hardwood species in eastern North America. Yet, its genomic diversity and adaptive structure remain poorly characterized. Using genotyping-by-sequencing (GBS), we generated 20,847 single nucleotide polymorphisms (SNPs) from 843 individuals sampled across 72 populations spanning the species' native range. Population and landscape genomic analyses revealed a broadly homogenous pattern of genetic variation, with weak but significant population structure, predominantly shaped by neutral processes, including postglacial demographic history and extensive historical gene flow. To detect signatures of local adaptation, we combined FST-based outlier detection with genotype-environment association (GEA) approaches. Across four genome scan methods, 142 SNPs were identified by at least two analytical approaches. Although temperature-related variables, particularly extreme minimum temperature (EMT), and moisture indices (MSP, SHM) showed significant associations with allele frequency variation, climate explained only a small fraction of total genomic variance. These results indicate that adaptive signals in Q. rubra are detectable but weak, consistent with polygenic adaptation involving small allele-frequency shifts. Together, our findings suggest that Q. rubra likely combines a polygenic genomic background with high within-population genetic diversity and inferred phenotypic plasticity rather than strict local adaptation to cope with environmental changes. This study provides a genomic foundation for Q. rubra and creates resources to support conservation planning, breeding programs, and the development of genomic traceability tools for provenance verification.

Forest trees are foundation species of many ecosystems and are challenged by global environmental changes. We assemble genetic facts and arguments supporting or undermining resilient responses of forest trees to those changes. Genetic resilience is understood here as the capacity of a species to restore its adaptive potential following environmental changes and disturbances. Importantly, the data come primarily from European temperate tree species with large distributions and consider only marginally species with small distributions. We first examine historical trajectories of trees during repeated climatic changes. Species that survived the Pliocene-Pleistocene transition and underwent the oscillations of glacial and interglacial periods were equipped with life history traits enhancing persistence and resilience. Evidence of their resilience also comes from the maintenance of large effective population sizes across time and rapid microevolutionary responses to recent climatic events. We then review genetic mechanisms and attributes shaping resilient responses. Usually, invoked constraints to resilience, such as genetic load or generation time and overlap, have limited consequences or are offset by positive impacts. Conversely, genetic plasticity, gene flow, introgression, genetic architecture of fitness-related traits and demographic dynamics strengthen resilience by accelerating adaptive responses. Finally, we address the limitations of this review and highlight critical research gaps.

Le changement climatique, dont le rythme semble s’accélérer, amène régulièrement au centre de l’actualité un cortège de conséquences plus ou moins directes dans le domaine agricole. Quand certaines régions sont en proie à des sécheresses récurrentes et au manque d’eau, d’autres voient leurs conditions climatiques devenir un peu plus clémentes, interrogeant sur les possibilités d’un déplacement géographique de certaines cultures (le vin de Bordeaux finira-t-il par être produit en Cornouailles ?). Un tel déplacement pourrait se produire par choix et par action humaine (on irait planter les espèces concernées ailleurs), mais pourrait-il aussi se faire naturellement, au gré de l’évolution biologique des végétaux en réaction aux nouvelles conditions climatiques ? Pour répondre à une telle question, il faut disposer d’éléments de comparaison sur très longue période (remontant aux évolutions climatiques antérieures) et portant sur des espèces végétales à longue vie et évolution lente, dont on a pu apprécier le comportement au fil du temps. À cet égard, les arbres (et les forêts qu’ils composent) constituent un objet d’observation particulièrement intéressant, que nous présente Antoine Kremer dans cet article, à partir du cas des chênes tempérés. En effet, à la lumière de l’histoire évolutive des arbres (leur migration au fil du temps, la sélection naturelle, leur résilience, leur adaptation, leur génétique), on peut apprécier leur capacité à faire face aux changements climatiques, individuellement comme collectivement. Ceci permet, comme le souligne Antoine Kremer dans un second temps, d’en tirer divers enseignements pour la gestion forestière : en matière d’assistance à la migration des espèces, de temporalité de la gestion sylvicole, de composition des forêts, etc. À l’heure où l’on entend parler plus fréquemment de mortalité d’espèces et de changements génétiques dans les forêts, les connaissances relatives à l’évolution biologique des arbres apportent de nouveaux éléments à prendre en compte dans l’adaptation au changement climatique. S.D.

Closely related species often use the same genes to adapt to similar environments. However, we know little about why such genes possess increased adaptive potential and whether this is conserved across deeper evolutionary lineages. Adaptation to climate presents a natural laboratory to test these ideas, as even distantly related species must contend with similar stresses. Here, we re-analyse genomic data from thousands of individuals from 25 plant species as diverged as lodgepole pine and Arabidopsis (similar to 300 Myr). We test for genetic repeatability based on within-species associations between allele frequencies in genes and variation in 21 climate variables. Our results demonstrate significant statistical evidence for genetic repeatability across deep time that is not expected under randomness, identifying a suite of 108 gene families (orthogroups) and gene functions that repeatedly drive local adaptation to climate. This set includes many orthogroups with well-known functions in abiotic stress response. Using gene co-expression networks to quantify pleiotropy, we find that orthogroups with stronger evidence for repeatability exhibit greater network centrality and broader expression across tissues (higher pleiotropy), contrary to the 'cost of complexity' theory. These gene families may be important in helping wild and crop species cope with future climate change, representing important candidates for future study.

Central European white oaks expanded rapidly after the last glacial period and reached their current distribution range during the early Holocene. They have been an important resource of timber, fuelwood and animal feed for humans, who actively promoted their presence in forests and other landscape types at least since the early historical times. Besides stands with intensive management, putatively relict populations of three native oak species can be found on unproductive sites with restricted accessibility. Here, we apply chloroplast and nuclear microsatellite markers in order to address the autochthony of relict and managed stands and compare the spatial distribution of genetic variation between them. Based on data from more than 150 populations, we demonstrate that oak autochthony was preserved throughout historical times which is likely the result of traditional silvicultural treatment. This is supported by the fact that the spatial pattern of chloroplast haplotype distribution still reflects the post-glacial recolonization in both relict and old managed stands. We observed significant admixture of haplotypes only in stands established after the Second World War, which is attributable to the transfer of reproductive material used for afforestation. In terms of nuclear genetic variation, we observed marked differences among species. Quercus pubescens exhibited a pronounced genetic structure. Genetic drift and limited gene flow among its small and isolated populations in our study area might have contributed to this pattern. Varying extent of genetic introgression with other sympatric oak species could offer an additional explanation. On the contrary, the gene pools of Q. petraea and Q. robur are highly homogenous, displaying only weak isolation-by-distance. We found no significant differences of genetic diversity and differentiation between relict and managed stands. This suggests that seed transfer mostly occurred within our study area, even in those stands established in post-war times, verifying previous findings which point out limited human interference. We recommend consideration of population genetic structure for gene conservation, with a finer resolution of gene conservation units needed for Q. pubescens due to its spatial genetic structure. Both relict and old managed stands, species-pure or mixed, are suitable for conservation, as they host autochthonous gene pools. Coppice-with-standard management could contribute to preservation of autochthony. In the face of climate change, it is also important to maintain the evolutionary potential of the stands, by facilitating generative reproduction and allowing for hybridization in mixed stands.

Key message Mining genome-wide DNA sequences enabled the discovery of near-diagnostic markers for species assignment in four European white oaks (Quercus petraea (Matt.) Liebl., Quercus pubescens Willd., Quercus pyrenaica Willd., and Quercus robur L.) despite their low interspecific differentiation. Near-diagnostic markers are almost fully fixed in one species and absent in the three others. As a result, only a handful of markers are needed for species identification, making this genetic assay a very promising operational taxonomic assignment procedure in research and forestry. Context Identifying species in the European white oak complex has been a long-standing concern in taxonomy, evolution, forest research, and management. Quercus petraea (Matt.) Liebl., Q. robur L., Q. pubescens Willd., and Q. pyrenaica Willd. are part of this species complex in western temperate Europe and hybridize in mixed stands, challenging species identification. Aims Our aim was to identify near-diagnostic single-nucleotide polymorphisms (SNPs) for each of the four species that are suitable for routine use and rapid diagnosis in research and applied forestry. Methods We first scanned existing whole-genome and target-capture data sets in a reduced number of samples (training set) to identify candidate diagnostic SNPs, i.e., genomic positions being characterized by a reference allele in one species and by the alternative allele in all other species. Allele frequencies of the candidates SNPs were then explored in a larger, range-wide sample of populations in each species (validation step). Results We found a subset of 38 SNPs (10 for Q. petraea, 7 for Q. pubescens, 9 for Q. pyrenaica, and 12 for Q. robur) that showed near-diagnostic features across their species distribution ranges with Q. pyrenaica and Q. pubescens exhibiting the highest (0.876) and lowest (0.747) diagnosticity, respectively. Conclusions We provide a new, efficient, and reliable molecular tool for the identification of the species Q. petraea, Q. robur, Q. pubescens, and Q. pyrenaica, which can be used as a routine tool in forest research and management. This study highlights the resolution offered by whole-genome sequencing data to design near-diagnostic marker sets for taxonomic assignment, even for species complexes with relatively low differentiation.

Climate change threatens the role of European forests as a long-term carbon sink. Assisted migration aims to increase the resilience of forest tree populations to climate change, using species-specific climatic limits and local adaptations through transferring seed provenances. We modelled assisted migration scenarios for seven main European tree species and analysed the effects of species and seed provenance selection, accounting for environmental and genetic variations, on the annual above-ground carbon sink of regrowing juvenile forests. To increase forest resilience, coniferous trees need to be replaced by deciduous species over large parts of their distribution. If local seed provenances are used, this would result in a decrease of the current carbon sink (40 TgC yr−1) by 34–41% by 2061–2080. However, if seed provenances adapted to future climates are used, current sinks could be maintained or even increased to 48–60 TgC yr−1.

Specialized or secondary metabolites play a key role in plant resistance against abiotic stresses and defences against bioaggressors. For example, in sessile oaks Quercus petraea , phenolics contribute to reduce herbivore damage and improve drought resistance. Here, we explored the natural variation of specialized metabolites in nine European provenances of sessile oaks and aimed to detect its underlying genetic bases. We sampled mature leaves from high and low branches on 225 sessile oak trees located in a common garden and used untargeted metabolomics to characterise the variation of 217 specialized metabolites. In addition, we used whole genome low-depth sequencing to genotype individuals for 1.4M genetic markers. We found that leaf specialized metabolites displayed extensive within-provenance variation, but very little differentiation between provenances. In addition, a genome-wide association study allowed detecting significant associations for 42% of these metabolites. Hence, our results suggest that genetic variation for most leaf specialized metabolites is unlikely to be locally adaptive, however lack of differentiation among populations suggests selection acts locally to maintain diversity at loci associated with leaf specialized metabolites variation.

Closely-related species often use the same genes to adapt to similar environments 1,2 . However, we know little about why such genes possess increased adaptive potential, and whether this is conserved across deeper evolutionary time. Classic theory suggests a “cost of complexity”: adaptation should occur via genes affecting fewer traits to reduce deleterious side-effects (i.e. lower pleiotropy) 3 . Adaptation to climate presents a natural laboratory to test this theory, as even distantly-related species must contend with similar stresses 4 . Here, we re-analyse genomic data from thousands of individuals from 25 plant species to identify a suite of 108 genes enriched for signatures of repeated local adaptation to climate. This set includes many genes with well-known functions in abiotic stress response, identifying key genes that repeatedly drive adaptation in species as distantly-related as lodgepole pine and Arabidopsis (~ 300 My). Using gene co-expression networks to quantify each gene’s pleiotropy, we find enrichment for greater network centrality/interaction strength and broader expression across tissues (i.e. higher pleiotropy), contrary to the ”cost of complexity” theory. These genes may be particularly important in helping both wild and crop species cope with future climate change, representing a set of important candidates for future study.

Background Global warming raises serious concerns about the persistence of species and populations locally adapted to their environment, simply because of the shift it produces in their adaptive landscape. For instance, the phenological cycle of tree species may be strongly affected by higher winter temperatures and late frost in spring. Given the variety of ecosystem services they provide, the question of forest tree adaptation has received increasing attention in the scientific community and catalyzed research efforts in ecology, evolutionary biology and functional genomics to study their adaptive capacity to respond to such perturbations. Results In the present study, we used an elevation gradient in the Pyrenees Mountains to explore the gene expression network underlying dormancy regulation in natural populations of sessile oak stands sampled along an elevation cline and potentially adapted to different climatic conditions mainly driven by temperature. By performing analyses of gene expression in terminal buds we identified genes displaying significant dormancy, elevation or dormancy-by-elevation interaction effects. Our Results highlighted that low- and high-altitude populations have evolved different molecular strategies for minimizing late frost damage and maximizing the growth period, thereby increasing potentially their respective fitness in these contrasting environmental conditions. More particularly, population from high elevation overexpressed genes involved in the inhibition of cell elongation and delaying flowering time while genes involved in cell division and flowering, enabling buds to flush earlier were identified in population from low elevation. Conclusion Our study made it possible to identify key dormancy-by-elevation responsive genes revealing that the stands analyzed in this study have evolved distinct molecular strategies to adapt their bud phenology in response to temperature.

Previous theory has shown that assortative mating for plastic traits can maintain genetic divergence across environmental gradients despite high gene flow. Yet these models did not examine how assortative mating affects the evolution of plasticity. We here describe patterns of genetic variation across elevation for plasticity in a trait under assortative mating, using multiple-year observations of budburst date in a common garden of sessile oaks. Despite high gene flow, we found significant spatial genetic divergence for the intercept, but not for the slope, of reaction norms to temperature. We then used individual-based simulations, where both the slope and the intercept of the reaction norm evolve, to examine how assortative mating affects the evolution of plasticity, varying the intensity and distance of gene flow. Our model predicts the evolution of either suboptimal plasticity (reaction norms with a slope shallower than optimal) or hyperplasticity (slopes steeper than optimal) in the presence of assortative mating when optimal plasticity would evolve under random mating. Furthermore, a cogradient pattern of genetic divergence for the intercept of the reaction norm (where plastic and genetic effects are in the same direction) always evolves in simulations with assortative mating, consistent with our observations in the studied oak populations.

Societal Impact Statement The rapidity of evolutionary changes in trees and whether this pace is sufficient to cope with ongoing climatic change are hotly debated issues in ecology today. Climate warming began in the mid‐19th century, after the Little Ice Age (LIA). Monitoring temporal genetic changes during this climatic transition in multicentennial oak populations revealed evidence of fluctuating selection and rapid evolution. These findings suggest that rapid evolution is probably also currently underway. They may lead to management options for operational forestry aiming to stimulate evolutionary mechanisms during the renewal of oak stands and to decrease potential temporal gene flow. Summary Retrospective studies of the evolutionary responses of tree populations to past documented climate change can provide insight into the adaptive responses of these organisms to ongoing environmental changes. We used a retrospective approach to monitor genetic changes over time in multicentennial sessile oak (Quercus petraea L.) forests. We compared the offspring of three age‐structured cohorts (340, 170, and 60 years old, dating from about 1680, 1850, and 1960) spanning the late Little Ice Age and early Anthropocene. The experiment was repeated in three different forests in western France. The offspring were raised in a common garden experiment, with 30 to 53 open‐pollinated families per cohort. We assessed 16 phenotypic traits in the common garden and observed significant shifts between cohorts for growth and phenology‐related traits. These shifts were correlated with differences in the prevailing temperatures in the past and could be interpreted as temporal genetic changes. However, there was no temporal trend for genetic variation. The genetic changes between the cold (late Little Ice Age) and warm (early Anthropocene) periods were mostly opposite for growth and phenology‐related traits. These findings highlight fluctuations of selection and a rapid evolutionary response of tree populations to climatic transitions in the past, suggesting that similar trends may be at work now. We discuss these results in terms of the mode and direction of evolution, and their potential implications for the adaptive management of oak forests.

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.

Knowing which drivers affect the spatial distribution of hybridizing species and their admixed individuals on local or regional scale can leverage our understanding about processes that shape taxonomic diversity. Hybridizing white oak species ( Quercus sect. Quercus ) represent an ideal study system to elucidate which environmental factors determine their relative abundance and admixture levels within admixed forest stands. To elaborate these relationships, we used 58 species-diagnostic single-nucleotide polymorphism (SNP) markers and high-resolution topographic and soil data to identify the environmental factors associated with taxonomic composition of individuals and populations in 15 mixed stands of Q. petraea and Q. pubescens in the Valais, an inner-Alpine valley in Switzerland. At the individual tree level, generalized linear models (GLMs) explained a relatively small part of variation ( R 2 = 0.32). At the population level, GLMs often explained a large part of variation ( R 2 = 0.54–0.69) of the taxonomic indices. Mean taxonomic composition of the sites depended mainly on altitude and geographic position. Moreover, the more within-site variation we found in predictors related to topographic position, the higher was the average genetic admixture of single trees. Our results show that a multitude of topographic and edaphic factors affect the taxonomic composition and admixture levels of these two hybridizing oak species on local scale and that regional heterogeneity of these factors promote taxonomic diversity and admixture. Overall, our study highlights the prospects of using tailored genetic resources and high-resolution environmental data to understand and predict taxonomic composition in response to changing environments.

Key message Sessile oak ( Quercus petraea (Matt.) Liebl.) provenance variation was assessed in a multisite test based on traits of economic and ecological relevance in France. While climatic drivers generated genetic clines at a range-wide scale, provenance variation in France was mainly shaped by past silvicultural regimes. We developed a multitrait approach to facilitate decision-making for seed sourcing. A set of provenance clusters is proposed, supporting recommendations for plantation programmes. Context Among broadleaves, sessile oak ( Quercus petraea) is likely to spread in the context of current climate change and is increasingly planted in France. Seed sourcing is of the utmost importance for ensuring plantation success and adaptation. The selection of appropriate seed sources is highly challenging when the future climate conditions of plantation areas are uncertain. Aims We aimed at identifying drivers of provenance variation in Q. petraea and to build provenance clusters based on traits of adaptive and economic value, to ultimately support decision-making in seed sourcing. Methods We analysed a multisite provenance test established 30 years ago and comprising a large collection of Q. petraea provenances by performing phenotypic assessments of survival, growth, phenology, and stem-quality traits. We analysed climate-trait correlations at a range-wide scale and used multivariate statistics [multivariate mixed models, principal component analysis (PCA)] and classification methods [hierarchical clustering analysis (HCA), K-means method] to generate an overall clustering of french provenances. Results Provenance effects were highly significant regardless of the trait considered, whereas interaction effects between provenance and other experimental sources of variation were minor compared to provenance and environmental variance. There was limited variation between provenances collected in the same forest in comparison to origins of different forests. We found sharp temperature-driven genetic clines for growth and phenology-related traits at a range-wide scale. The multitrait classification approach grouped the French provenances into 11 clusters, with the members of each cluster having similar trait values. Overall, the cluster composition of provenances poorly matched the provenance regions identified on ecological grounds, but rather mirrored the silvicultural regimes implemented in the source stands in the past. Conclusions Two of the provenance clusters (comprising a total of 34 provenances) were identified as potentially useful sources of reproductive material. We recommend mixing seeds of different provenances from a given cluster to ensure the maintenance of diversity and to enhance adaptability to future climatic conditions.