Rapid global climate change is posing a substantial threat to biodiversity. The assessment of population vulnerability and adaptive capacity under climate change is crucial for informing conservation and mitigation strategies. Here we generate a chromosome-scale genome assembly and re-sequence genomes of 230 individuals collected from 24 populations for Populus koreana, a pioneer and keystone tree species in temperate forests of East Asia. We integrate population genomics and environmental variables to reveal a set of climate-associated single-nucleotide polymorphisms, insertion/deletions and structural variations, especially numerous adaptive non-coding variants distributed across the genome. We incorporate these variants into an environmental modeling scheme to predict a highly spatiotemporal shift of this species in response to future climate change. We further identify the most vulnerable populations that need conservation priority and many candidate genes and variants that may be useful for forest tree breeding with special aims. Our findings highlight the importance of integrating genomic and environmental data to predict adaptive capacity of a key forest to rapid climate change in the future.

Despite widespread biodiversity loss, our understanding of how species and populations will respond to accelerated climate change remains limited. In this study, we integrate population genomics, experimental evolution, and environmental modeling to elucidate the evolutionary responses to climate change in Populus lasiocarpa, a key alpine forest tree species primarily distributed in the mountainous regions of a global biodiversity hotspot. Over historical timescales, our findings demonstrate that demographic dynamics, divergent selection, and long-term balancing selection have shaped and maintained genetic variation within and between populations. In examining genomic signatures of contemporary climate adaptation, we found that haplotype blocks, potentially caused by inversion polymorphisms that suppress recombination, are linked to enriched combinations of locally adaptive environmental variations. We further assessed the relative contributions of environmentally induced plastic responses, constitutive expression divergence between genetic clusters, and their interactions in driving gene expression variation and divergence. Notably, we observed a strong correlation between sequence divergence and constitutive differential expression among genetic clusters. Finally, by incorporating genetic adaptation, migration, and genetic load into our predictions of population-level climate change risks, we identified western populations-primarily distributed in the Hengduan Mountains, a region known for its environmental heterogeneity and significant biodiversity—as the most vulnerable to climate change. These populations should be prioritized for conservation and management. Overall, our study advances the understanding of the relative roles of long-term natural selection, local environmental adaptation, and immediate plastic expression changes in shaping the responses of natural populations of keystone species to climate change.

Rapid global climate change is posing a huge threat to biodiversity. Assessments of the adaptive capacity for most taxa is usually performed on the species as a whole, but fails to incorporate intraspecific adaptive variation that may play a fundamental role in buffering future shifting climates. Here we generate a chromosome-scale genome assembly for Populus koreana , a pioneer and keystone tree species in East Asia temperate forests. We also obtain whole-genome sequences of 230 individuals collected from 24 natural populations. An integration of population genomics and environmental variables was performed to reveal the genomic basis of local adaptation to diverse climate variable. We identify a set of climate-associated single nucleotide polymorphisms (SNPs), insertions-deletions (Indels) and structural variations (SVs), in particular numerous adaptive non-coding variants distributed across the genome of P. koreana . We incorporate these variants into an environmental modelling scheme to predict spatiotemporal responses of P. koreana to future climate change. Our results highlight the insights that the integration of genomic and climate data can shed on the future evolutionary adaptive capacities of a species to changing environmental conditions.

Characterizing genomic variation in keystone forest trees is critical for understanding and predicting the adaptation and maladaptation of terrestrial ecosystems to global climate change. In this study, we integrate five high-quality genomes and high-depth whole-genome resequencing data from 222 individuals across 44 natural populations of Populus davidiana in East Asia. Our findings reveal that genome divergence strongly correlates with epigenetic and regulatory features, with variable genomic regions closely associated with dynamic transposon activity linked to epigenetic modifications. A population-scale genotype-environment association analysis identifies 10,372 adaptive single nucleotide polymorphisms (SNPs) and 1322 adaptive structural variations (SVs). Among these, a temperature-associated SV and a precipitation-associated SV undergo functional validation providing evidence of their roles in the expression of PdaMSL10, a mechanosensitive ion channel, and the transcription factor PdaWRKY40, respectively. Overexpression and RNAi experiments demonstrate that differential expression of PdaWRKY40 is strongly associated with drought sensitivity or tolerance, facilitating adaptation to diverse environmental conditions. Additionally, genomic vulnerability forecasts under future climate scenarios highlight the increasingly significant role of SVs in environmental adaptation. These findings advance our understanding of the genetic mechanisms underlying climate adaptation in non-model keystone species and provide invaluable genetic resources for breeding programs aimed at enhancing climate resilience.