Search bioRxiv⌕ Search

Biology subjects

Sork, V. L.

Publications and source records attributed to Sork, V. L..

9 recordsLinked to original sources

Canopy traits reveal climate-associated genetic differentiation in a California oak common garden

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.

evolutionary biology↗

Is epigenetics Lamarck's revenge? The evolutionary and ecological impacts of DNA methylation in a California oak

DNA methylation, an epigenetic mechanism, 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 two common gardens in both gardens. Still, overall 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 potential importance for the ecological and evolutionary responses of long-lived trees to environmental change.

evolutionary biology↗

Climate of origin constrains phenological tracking of temperature in a California endemic oak (Quercus lobata)

Premise of the study. Phenotypic plasticity is advantageous for many plants that experience environmental fluctuations, but strong selection pressures can establish limits to plasticity. In deciduous trees, the ability to time leaf elongation in response to spring temperatures can extend the length of the growing season for a given year's climate. However, emergence timing may have undergone strong selection by factors like cold temperatures, limiting the capacity of locally adapted populations to adjust via plasticity to new conditions. Methods. Using a nine-year dataset of 659 families of Quercus lobata in two common gardens, we tested how climate of origin and annual temperatures at the gardens affected variation in phenology. We then examined whether leaf emergence timing was under selection in the gardens by testing its effects on growth. Finally, we tested whether among-year plasticity in leaf emergence timing conferred a growth benefit. Key results. Year-to-year environmental variation explained more phenological variation than genetic differences associated with climate of origin, yet trees from cooler climates were more constrained in their ability to track temperature than trees from warmer climates. We found evidence of weak stabilizing and directional selection on phenology, suggesting that strong selection in favor of earlier phenology is unlikely. Finally, we found no evidence that selection has favored increased plasticity in Q. lobata. Conclusions. Phenological plasticity remains a key driver of plants' response to changing temperatures, but it is constrained by natural selection. As temperatures rise, these processes may disproportionately limit the ability of trees adapted to cooler climates to shift their phenology to match spring temperatures.

plant biology↗

Persistent adaptational lag to climate threatens future tree populations, but phenotype-informed assisted gene flow can mitigate its effects

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.

ecology↗

Current maladaptation increases with age in valley oak (Quercus lobata): Implications for future populations

Adaptation and maladaptation are two fundamental evolutionary processes shaping the success of tree populations. Local adaptation has been studied extensively, but maladaptation, which not simply be the inverse, is particularly important for long-lived species since human impact is changing the environment on a very short time scale. Because maladaptation may be observed at different stages of an organisms life cycle, temporal variation may reduce or enhance the vulnerability of a species to a new climate environment. In this paper, we use findings from an ongoing range-wide provenance study comprising two common gardens of 3,674 half-sib juvenile valley oaks (Quercus lobata) from 658 maternal families to address two objectives. First, we test whether maladaptation (a) persists as trees age and/or (b) varies in magnitude over time. We model growth rates and performance measures (height * survival; "performance") across families sourced from sites with differing climates. Second, we assess the extent to which evidence-based seed transfer can mitigate the impact of maladaptation. We find that the twelve-year-old trees are currently adapted to temperatures not only cooler than their home site, but also beyond the coolest limit of the current species range. Moreover, this maladaptive pattern is exacerbated in hotter years of our study. Despite a general pattern of maladaptation, we demonstrate the feasibility of using phenotype-informed seed transfer guidelines for replanting trees in current populations by identified high-performing individuals from varied environmental origins. Overall, our results indicate that valley oak is imperiled by current and future climate conditions, but high-performing trees well suited to sites across the species range can be identified as seed donors. We conclude that current maladaptation in a long-lived tree species is a major threat that is first apparent within a few years and worsens as trees age, but careful management of vulnerable oak populations can improve their resiliency.

evolutionary biology↗

Drought-associated genes exhibit high constitutive expression in Quercus douglasii, a drought tolerant California oak

Drought stress is a strong selective pressure for all plant species. Plants can respond to water shortage through various strategies that confer drought tolerance, but with a potential cost for growth. 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 population in the Sierra Nevada Foothills in California. In the greenhouse, we subjected 24 seedlings from six 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 down-regulated 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. Up-regulated genes were related to known drought response functions, while down-regulated 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 drought sensitive oak, which a novel finding for drought tolerance strategies in tree species. We conclude that the drought tolerant strategy of Q. douglasii incorporates high constitutive expression levels of drought-responsive genes, as well as some plasticity in its response once environmental stress is experienced.

plant biology↗

Maladaptive response of an endemic California oak to climatic warming is previewed by interannual variation in growth and survival

Climate change poses a major threat to long-lived tree populations by shifting environmental conditions away from those to which species are adapted. One of the biggest concerns is that individuals that are adapted to current conditions will become maladapted to new conditions due to a reduction in fitness. If tree populations are already maladapted to their current environments, climate change may put them at even greater risk. Valley oak (Quercus lobata), a foundational California endemic tree species, has already lost much of its range to anthropogenic activities and has been shown to demonstrate patterns of climatic maladaptation. Given the rapid pace of climate change, predicting the future of a species requires quantifying the extent to which contemporary populations are adapted or maladapted to current climates. Here, we tested the extent and variability of maladaptation in valley oak using a ten-year, range-wide provenance study of 3,371 half-sib juvenile trees from 658 maternal lineages. We compared growth rates and multiplicative fitness functions (height * survival; MFF) across families sourced from sites with differing climates relative to the gardens, as well as against annual phenological records. We found evidence that valley oak trees are most adapted to temperatures beyond the coolest limit of the current species range. Within and across years, trees sourced from hotter localities had higher growth and fitness in the gardens, and the relationship was more pronounced in hotter years. Trees showed persistent maladaptation after ten years, suggesting that the role of phenotypic plasticity in immediate environmental response is superseded by underlying genotypes. Finally, trees with earlier leaf phenology (associated with warmer source climates) consistently showed higher growth rates, further demonstrating a maladaptive pattern. Our results suggest that short-term variation in fitness shows immediate short-term response to climate warming, "previewing" a concerning range of species-level responses to increasing temperature.

evolutionary biology↗

High-quality genome and methylomes illustrate features underlying evolutionary success of oaks

The genus Quercus, which emerged ~55 million years ago during globally warm temperatures, diversified into ~450 species. We present a high-quality de novo genome assembly of a California endemic oak, Quercus lobata, revealing features consistent with oak evolutionary success. Effective population size remained large throughout history despite declining since the early Miocene. Analysis of 39,373 mapped protein-coding genes outlined copious duplications consistent with genetic and phenotypic diversity, both by retention of genes created during the ancient{gamma} whole genome hexaploid duplication event and by tandem duplication within families, including the numerous resistance genes and also unexpected candidate genes for an incompatibility system involving multiple non-self-recognition genes. An additional surprising finding is that subcontext-specific patterns of DNA methylation associated with transposable elements reveal broadly-distributed heterochromatin in intergenic regions, similar to grasses (another highly successful taxon). Collectively, these features promote genetic and phenotypic variation that would facilitate adaptability to changing environments.

genomics↗

Genomic landscape of the global oak phylogeny

O_LIThe tree of life is highly reticulate, with the history of population divergence buried amongst phylogenies deriving from introgression and lineage sorting. In this study, we test the hypothesis that there are regions of the oak (Quercus, Fagaceae) genome that are broadly informative about phylogeny and investigate global patterns of oak diversity.\nC_LIO_LIWe utilize fossil data and restriction-site associated DNA sequencing (RAD-seq) for 632 individuals representing ca. 250 oak species to infer a time-calibrated phylogeny of the worlds oaks. We use reversible-jump MCMC to reconstruct shifts in lineage diversification rates, accounting for among-clade sampling biases. We then map the > 20,000 RAD-seq loci back to a recently published oak genome and investigate genomic distribution of introgression and phylogenetic support across the phylogeny.\nC_LIO_LIOak lineages have diversified among geographic regions, followed by ecological divergence within regions, in the Americas and Eurasia. Roughly 60% of oak diversity traces back to four clades that experienced increases in net diversification due to climatic transitions or ecological opportunity.\nC_LIO_LIThe support we find for the phylogeny contrasts with high genomic heterogeneity in phylogenetic signal and introgression. Oaks are phylogenomic mosaics, and their diversity may in fact depend on the gene flow that shapes the oak genome.\nC_LI

evolutionary biology↗