Victoria L. Sork

Background and Aims. Phenotypic variation in plant populations reflecting historical climate adaptation may affect performance under future climates. In long-lived trees, height and stem diameter are commonly used to assess growth, but these measures may not fully capture complementary structural and functional dimensions of performance, such as canopy development and vigor. We investigated whether canopy traits reveal climate-associated genetic differentiation in Quercus lobata. Methods. Using drone-based remote sensing of 1,395 12-year-old Quercus lobata trees from 601 families in a common garden, we quantified canopy volume and greenness, using the Normalized Difference Vegetation Index (NDVI). Previous analyses indicated that trees originating from warmer climates grew more in common gardens than those from cooler climates. To assess whether canopy traits showed similar patterns, we tested for family-level variation in each trait and associations with climate of origin. Key Results. Canopy volume and greenness showed significant genetic variation among families and significant associations with climate of origin. Trees from hotter climates had greater canopy volume and greenness than trees from cooler climates. Conclusions. These covarying traits provide novel evidence of climate-associated genetic differentiation in tree performance, consistent with historical climate selection. Trees originating from climates with hot summers, moderate winters, and low precipitation performed best in the garden, suggesting that they will perform better than trees adapted to cool, wet conditions under future climate change.

Summary: Epigenetics has been proposed as a basis for Lamarckian inheritance of acquired characteristics. This hypothesis raises questions about environmental induction of DNA methylation, its persistence across generations, and associations with gene expression. We investigated these processes in the California oak, Quercus lobata . Based on 40 range-wide adult trees and their progeny grown in two common gardens, we tested four predictions: (i) DNA methylation is environmentally induced; (ii) methylation shows parent-offspring correspondence; (iii) environmentally induced patterns remain stable after transmission; and (iv) DNA methylation is associated with gene expression, varying by sequence context and TE proximity. Using methylomes and transcriptomes, we found support for all predictions except the third: CHH methylation was environmentally induced, but rarely showed parent-offspring correspondence, whereas CG methylation showed the opposite pattern. DNA methylation was associated with gene expression, depending on the sequence context and proximity to TEs. We identified one stress-associated gene with environmentally responsive CHH methylation that showed parent–offspring correspondence in both gardens. Still, our evidence for Lamarckian-like evolution is not compelling. Nevertheless, DNA methylation was environmentally responsive, showed parent–offspring correspondence, and was associated with gene expression, highlighting its importance for the ecological and evolutionary responses of long-lived trees to environmental change.

Tree populations are threatened by a multitude of human activities ranging from deforestation to air pollution. Rapid climate change, including warmer temperatures and increased drought frequency, poses a particular threat by reducing photosynthesis and growth, increasing susceptibility to pests and disease, and intensifying risk of mortality. To maintain healthy forests in the future, resource managers could benefit from practical tools to identify vulnerable populations and select appropriate seed sources for restoration and reforestation. In this paper, we outline four recently developed genomic approaches that can help guide these assessments. First, combining long-term growth data from provenance studies with genetic information makes it possible to identify traits associated with better performance under warmer climates, allowing managers to select climate-adapted planting material. Second, analyzing how genetic variation changes across climate gradients can highlight which tree stands may be most at risk under future conditions. Third, experimental studies on seedlings can identify genes involved in stress responses, improving our ability to predict how different populations will respond to climate change. Fourth, epigenetic markers, which are chemical changes to DNA that can influence gene activity, may provide early indicators of stress that may help identify vulnerable populations and resilient seed sources. As climate change accelerates, these genomic and computational tools offer new opportunities for informed, forward-looking management strategies for forest conservation and restoration.

Climate change is threatening crop yield of a broad range of agricultural species, impacting global food security and trade. Crop wild relatives may contain climate adaptations that can be quickly introduced into cultivars, especially in perennial tree crops that use rootstock. Identifying climate resilient genotypes that can potentially be used as alternative rootstock is imperative to mitigate the impacts of climate change. Here, we used whole genome sequence data of 59 wild Juglans hindsii (Northern California black walnut) and 39 wild J. californica (Southern California black walnut) adult trees to: (i) determine predicted adaptedness to future climate based on landscape genomic models, (ii) explore their adaptedness if used as rootstock in existing walnut orchards and (iii) identify potential future planting sites within existing croplands. Wild J. hindsii has the highest predicted adaptedness to the future climate of Northern and Central California walnut orchards, while wild J. californica has the highest predicted adaptedness to Southern and Central California walnut orchards. Juglans californica has high adaptedness to the future climate of more existing cropland than J. hindsii does. If walnut farmers wanted to test new rootstock sources for their existing orchards or convert their farmland into walnut orchards, this study informs the exploration of such ideas. We illustrate how landscape genomic tools can be utilized in agricultural contexts as first steps in identifying climate adapted genotypes.

Habitat destruction and climate change are two primary drivers of global biodiversity loss. Many contemporary ecological preserves and preserve networks are designed to protect species and the ecological and evolutionary processes that will maintain future biodiversity. However, it is challenging to identify where to locate preserves and how to manage them to meet these goals. One emerging conservation tool is landscape genomics, which allows us to identify populations that may be maladapted to future climate and thereby helps prioritize areas for acquisition (areas of high adaptedness), restoration (areas of low adaptedness), and management. Here, using whole genome sequence data of 171 adult trees, we studied the climate adaptedness of California populations of coast live oak ( Quercus agrifolia ), a foundation species that broadly supports biodiversity, to develop a conservation management strategy, including direct acquisition, land management, and restoration that addresses the predicted impact of future climate. Over the range of coast live oak, we find that the northernmost and southernmost stands are predicted to be more at risk for maladaptation to climate change, with the central coast of California containing stands with high adaptedness, including in unprotected areas that might benefit from protection. Using three large preserves (focal sites) managed by The Nature Conservancy (TNC), we illustrate how moving seeds from low to high elevation parts of preserves could benefit future populations range‐wide by increasing overall climate adaptedness. We discuss the different levels of risk across focal sites and apply our interpretations into TNC's 400,000 + −acre conservation holdings in California to sustain future populations of this foundational tree species. This study represents a unique collaboration between academic and applied conservation scientists to both assess levels of maladaptedness of a foundational tree to predicted climate change and also develop a genomic‐informed seed transfer program to improve adaptedness of future populations.

Hybridization is common among plant taxa and can lead to adaptive introgression, range expansion, and even island colonization. Patterns of hybridization in natural and disturbed populations can reflect a species' evolutionary history and elucidate patterns of human influence. On the Channel Islands, reports of hybrid oaks, such as Q. × macdonaldii Greene & Kellogg, and anomalous individuals that appear to be oaks typically found on the mainland, including Q. lobata Née, Q. douglasii Hook. & Arn., and Q. engelmannii Greene, raise questions about their origin and history on the islands. Here, we examine the validity of those reports by using nuclear and chloroplast whole genome sequence data to elucidate species identities. As expected, we find that Q. × macdonaldii individuals are hybrids between Q. lobata and the endemic Island Scrub Oak, Q. pacifica Nixon & C.H. Mull., but identify only one pure Q. lobata individual on the islands, whose chlorotype is related to trees in the Santa Ynez Valley of Santa Barbara County, CA. In addition, the trees thought to be Q. douglasii and Q. engelmannii are actually Q. pacifica × Q. douglasii and Q. pacifica × Q. engelmannii hybrids, respectively. These hybrids were determined to be F1 hybrids that exclusively have the chlorotype of Q. pacifica, indicating unidirectional hybridization with the Island Scrub Oak as the maternal parent. The lack of pure parental individuals raises the questions of where the pollen donors came from, when were they present on the islands, and why have they disappeared. The lack of backcrossed individuals or an F2 generation suggests the mainland species may not be adapted to Channel Island environments and probably do not represent an ancient population of these species on the islands. Instead, these findings are consistent with a more recent arrival, potentially supporting the notion that Indigenous Peoples brought the mainland species to the Channel Islands. Conservation managers should be aware of the presence of hybrid individuals that are morphologically indistinguishable from their parental species and consult Indigenous groups on the preservation of mainland species and their hybrids.

Environmental factors shape the distributions of organisms and their underlying patterns of genetic variation. When climate changes rapidly, organisms that are adapted to current environments may become maladapted to future climates. Long‐lived tree species are especially susceptible to climate maladaptation due to their sessile nature and long generation times. Understanding how foundational tree species will respond to future climate, both in adaptive ability and distribution shifts, is imperative for effective management and conservation of tree populations and the ecosystems they comprise. Here, we used whole genome sequences from 163 individuals of blue oak ( Quercus douglasii ) to determine predicted adaptedness, the degree to which an organism can survive and reproduce in future climate, based on landscape genomic models, compare those genomic predictions with ecological niche model predictions, and propose seed sourcing and restoration site strategies to increase the adaptedness of stands at preserves managed by The Nature Conservancy. Both ecological and genomic models predict that blue oak stands will be more susceptible to future climate along the Sierra Nevada basin, with patches of higher climate adaptedness along the central coast of California. To test whether management practices could increase adaptedness of blue oak stands, we examined the impact of seed source and restoration site choice on future stands. Regardless of restoration site category, our expectation held true that future maladaptation risk is reduced the most when using seed sources preadapted to the future climate of the restoration site. However, restoration sites containing stands with high habitat suitability and high climate adaptedness always did best. We conclude that strategic conservation and management strategies utilizing seed transfer from climate‐adapted stands may improve the future health of blue oak stands susceptible to future climate.

Maladaptation in foundational tree species can undermine ecosystem stability, but few studies have quantified its current magnitude or its consequences under ongoing climate change. Using a range-wide provenance test of valley oak ( Quercus lobata ), we tested whether historical climate warming has already produced temperature-driven climate–fitness mismatches, whether climatic extremes intensify these mismatches, and whether understanding these patterns can inform management. Growth and survival models from a 12-year common garden study revealed that trees performed best under summer temperatures cooler than their home climates, demonstrating persistent maladaptation to contemporary temperature maxima. This mismatch intensified during hotter years, indicating that climate variability amplifies fitness costs and that stressful years impose lasting effects. However, simulations of assisted gene flow showed that sourcing seeds from high-performing maternal families yields greater projected future performance than climate-matched sourcing across the species’ range. Together, these findings provide rare phenotypic evidence that maladaptation is already constraining a keystone tree species and show that phenotype-informed management can outperform climate-matched seed sourcing under further temperature increases.

Drought stress is a strong selective pressure for all plant species. Plants respond to water shortage through various strategies that confer drought tolerance. These strategies may be plastic responses that occur with the onset of stress or may comprise continuously expressed (constitutive) traits regardless of water availability. Here, we used RNA-seq to characterize transcriptional responses to dehydration in seedlings of a drought-tolerant oak, Quercus douglasii, from a local population in the Sierra Nevada Foothills in California. In the greenhouse, we subjected 24 seedlings from 6 maternal families to dry-down or well-watered treatments and prepared RNA libraries from tissue collected before and after each treatment (48 libraries). Our goals were to characterize the pattern of up- and downregulated genes in response to dehydration and to assess the extent to which this drought-tolerant species shows differential versus constitutive expression as a drought response strategy. We identified few differentially expressed genes in response to dehydration. Upregulated genes were related to known drought response functions, while downregulated genes were enriched for gene ontology terms related to growth and carbohydrate metabolism. We discovered high constitutive expression of many putatively drought-responsive genes that had been found to exhibit gene expression plasticity in a different oak species, which is drought-sensitive. This novel finding demonstrates the potential for constitutive expression of genes involved in drought stress to provide an additional mechanism of drought tolerance for some tree species, such as Q. douglasii.

- Drought is a major stressor for plants globally. Variation in gene expression patterns across species can provide critical evidence for the genomic basis of drought tolerance. - We paired comparative transcriptomics with functional trait measurements to identify genomic mechanisms associated with drought tolerance across six species from three oak clades in California, including a pair of species within each clade representing relatively mesic or xeric environments. We tested how plastic and constitutive gene expression patterns varied among species with contrasting drought tolerance traits. We also tested whether gene expression responses were decoupled from phylogenetic history, suggesting they have evolved multiple times as adaptations to species climate niches. - Species with drought-tolerant traits exhibited lower levels of gene expression plasticity during leaf dehydration than drought-sensitive species, but showed signatures of positive selection on constitutive gene expression. Drought-sensitive species across clades converged in their patterns of plastic gene expression during dehydration, diverging from their more closely related drought tolerant species, suggesting that repeated evolution has shaped plastic gene expression responses to drought. - Drought-tolerant oak species have evolved constitutive gene expression alongside drought tolerant functional traits, while drought-sensitive oak species have evolved similar plastic gene expression responses to drought.