Genome-Wide Variation in DNA Methylation Predicts Variation in Leaf Traits in an Ecosystem-Foundational Oak Species

Epigenetic modifications such as DNA methylation are a potential mechanism for trees to respond to changing environments. However, it remains controversial the extent to which DNA methylation impacts ecologically important traits that influence fitness. In this study, we used reduced-representation bisulfite sequencing to associate genomic and epigenomic variation with seven phenotypic traits related to growth, leaf function, and disease susceptibility in 160 valley oak (Quercus lobata) saplings planted across two common gardens in California. We found that DNA methylation was associated with a significant fraction of phenotypic variance in plant height, leaf lobedness, powdery mildew infection, and trichome density. Two of the seven traits were significantly associated with DNA methylation in the CG context, three traits were significantly associated with CHG methylation, and two traits were significantly associated with CHH methylation. Notably, controlling for genomic variation in SNPs generally reduced the amount of trait variation explained by DNA methylation. Our results suggest that DNA methylation may serve as a useful biomarker to predict phenotypic variation in trees, though it remains unclear the degree to which DNA methylation is a causal mechanism driving phenotypic variation in forest tree species.

Intraspecific variation in the relationship between weather and masting behavior in valley oak, Quercus lobata

Masting behavior — variable and synchronized reproduction by a population of plants — has long been recognized as correlating with weather. How and why weather conditions influence seed production is, however, poorly understood. We investigated the relationships between acorn production and both local weather and long-term climate in 10 populations across the geographic range of the valley oak (Quercus lobata Née), a California endemic that matures acorns in a single season. Acorn production was larger following a cold spring in the prior year and dry conditions in the winter and spring immediately preceding acorn maturation; similar patterns were also found, with minor differences, at all 10 individual sites. The strength of the relationships varied geographically in the case of the correlation between winter rainfall and annual acorn production, which was stronger (more negative) at wetter sites. Thus, in contrast to a recent study in Quercus petraea (Matt.) Liebl., weather had generally similar effects on acorn production throughout the range of Q. lobata. Similar to Q. petraea, however, the strength of the relationship between site-level annual acorn production and one of the weather factors affecting acorn production (winter rainfall in the case of Q. lobata) varied geographically in ways that may be related to differences among sites in the degree of pollen limitation. Understanding the mechanisms by which weather affects seed production is challenging but critical if we are to understand how climate change will affect masting behavior in the future.

Adaptational lag to temperature in valley oak (Quercus lobata) can be mitigated by genome-informed assisted gene flow

Climate change over the next century is predicted to cause widespread maladaptation in natural systems. This prediction, as well as many sustainable management and conservation practices, assumes that species are adapted to their current climate. However, this assumption is rarely tested. Using a large-scale common garden experiment combined with genome-wide sequencing, we found that valley oak (Quercus lobata), a foundational tree species in California ecosystems, showed a signature of adaptational lag to temperature, with fastest growth rates occurring at cooler temperatures than populations are currently experiencing. Future warming under realistic emissions scenarios was predicted to lead to further maladaptation to temperature and reduction in growth rates for valley oak. We then identified genotypes predicted to grow relatively fast under warmer temperatures and demonstrated that selecting seed sources based on their genotype has the potential to mitigate predicted negative consequences of future climate warming on growth rates in valley oak. These results illustrate that the belief of local adaptation underlying many management and conservation practices, such as using local seed sources for restoration, may not hold for some species. If contemporary adaptational lag is commonplace, we will need new approaches to help alleviate predicted negative consequences of climate warming on natural systems. We present one such approach, “genome-informed assisted gene flow,” which optimally matches individuals to future climates based on genotype–phenotype–environment associations.