Demographic History and Natural Selection Shape Patterns of Deleterious Mutation Load and Barriers to Introgression across Populus Genome.

Hybridization and resulting introgression are important processes shaping the tree of life and appear to be far more common than previously thought. However, how the genome evolution was shaped by various genetic and evolutionary forces after hybridization remains unresolved. Here we used whole-genome resequencing data of 227 individuals from multiple widespread Populus species to characterize their contemporary patterns of hybridization and to quantify genomic signatures of past introgression. We observe a high frequency of contemporary hybridization and confirm that multiple previously ambiguous species are in fact F1 hybrids. Seven species were identified, which experienced different demographic histories that resulted in strikingly varied efficacy of selection and burdens of deleterious mutations. Frequent past introgression has been found to be a pervasive feature throughout the speciation of these Populus species. The retained introgressed regions, more generally, tend to contain reduced genetic load and to be located in regions of high recombination. We also find that in pairs of species with substantial differences in effective population size, introgressed regions are inferred to have undergone selective sweeps at greater than expected frequencies in the species with lower effective population size, suggesting that introgression likely have higher potential to provide beneficial variation for species with small populations. Our results, therefore, illustrate that demography and recombination have interplayed with both positive and negative selection in determining the genomic evolution after hybridization.

Integrating evolutionary genomics of forest trees to inform future tree breeding amid rapid climate change.

Global climate change is leading to rapid and drastic shifts in environmental conditions, posing threats to biodiversity and nearly all life forms worldwide. Forest trees serve as foundational components of terrestrial ecosystems and play a crucial and leading role in combating and mitigating the adverse effects of extreme climate events, despite their own vulnerability to these threats. Therefore, understanding and monitoring how natural forests respond to rapid climate change is a key priority for biodiversity conservation. Recent progress in evolutionary genomics, driven primarily by cutting-edge multi-omics technologies, offers powerful new tools to address several key issues. These include precise delineation of species and evolutionary units, inference of past evolutionary histories and demographic fluctuations, identification of environmentally adaptive variants, and measurement of genetic load levels. As the urgency to deal with more extreme environmental stresses grows, understanding the genomics of evolutionary history, local adaptation, future responses to climate change, and conservation and restoration of natural forest trees will be critical for research at the nexus of global change, population genomics, and conservation biology. In this review, we explore the application of evolutionary genomics to assess the effects of global climate change using multi-omics approaches and discuss the outlook for breeding of climate-adapted trees.

Cryptic divergences and repeated hybridizations within the endangered "living fossil" dove tree (Davidia involucrata) revealed by whole genome resequencing.

The identification and understanding of cryptic intraspecific evolutionary units (lineages) are crucial for planning effective conservation strategies aimed at preserving genetic diversity in endangered species. However, the factors driving the evolution and maintenance of these intraspecific lineages in most endangered species remain poorly understood. In this study, we conducted resequencing of 77 individuals from 22 natural populations of Davidia involucrata, a "living fossil" dove tree endemic to central and southwest China. Our analysis revealed the presence of three distinct local lineages within this endangered species, which emerged approximately 3.09 and 0.32 million years ago. These divergence events align well with the geographic and climatic oscillations that occurred across the distributional range. Additionally, we observed frequent hybridization events between the three lineages, resulting in the formation of hybrid populations in their adjacent as well as disjunct regions. These hybridizations likely arose from climate-driven population expansion and/or long-distance gene flow. Furthermore, we identified numerous environment-correlated gene variants across the total and many other genes that exhibited signals of positive evolution during the maintenance of two major local lineages. Our findings shed light on the highly dynamic evolution underlying the remarkably similar phenotype of this endangered species. Importantly, these results not only provide guidance for the development of conservation plans but also enhance our understanding of evolutionary past for this and other endangered species with similar histories.

Genomic insights into local adaptation and future climate-induced vulnerability of a keystone forest tree in East Asia.

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.