Forest tree species adaptation to climate across biomes: Building on the legacy of ecological genetics to anticipate responses to climate change.

Intraspecific variation plays a critical role in extant and future forest responses to climate change. Forest tree species with wide climatic niches rely on the intraspecific variation resulting from genetic adaptation and phenotypic plasticity to accommodate spatial and temporal climate variability. A centuries-old legacy of forest ecological genetics and provenance trials has provided a strong foundation upon which to continue building on this knowledge, which is critical to maintain climate-adapted forests. Our overall objective is to understand forest trees intraspecific responses to climate across species and biomes, while our specific objectives are to describe ecological genetics models used to build our foundational knowledge, summarize modeling approaches that have expanded the traditional toolset, and extensively review the literature from 1994 to 2021 to highlight the main contributions of this legacy and the new analyzes of provenance trials. We reviewed 103 studies comprising at least three common gardens, which covered 58 forest tree species, 28 of them with range-wide studies. Although studies using provenance trial data cover mostly commercially important forest tree species from temperate and boreal biomes, this synthesis provides a global overview of forest tree species adaptation to climate. We found that evidence for genetic adaptation to local climate is commonly present in the species studied (79%), being more common in conifers (87.5%) than in broadleaf species (67%). In 57% of the species, clines in fitness-related traits were associated with temperature variables, in 14% of the species with precipitation, and in 25% of the species with both. Evidence of adaptation lags was found in 50% of the species with range-wide studies. We conclude that ecological genetics models and analysis of provenance trial data provide excellent insights on intraspecific genetic variation, whereas the role and limits of phenotypic plasticity, which will likely determine the fate of extant forests, is vastly understudied.

Role of population genetics in guiding ecological responses to climate.

Population responses to climate were assessed using 3-7 years height growth data gathered for 266 populations growing in 12 common gardens established in the 1980s as part of five disparate studies of Pinus contorta var. latifolia. Responses are interpreted according to three concepts: the ecological optimum, the climate where a population is competitively exclusive and in which, therefore, it occurs naturally; the physiological optimum, the climate where a population grows best but is most often competitively excluded; and growth potential, the innate capacity for growth at the physiological optimum. Statistical analyses identified winter cold, measured by the square root of negative degree-days calculated from the daily minimum temperature (MINDD01/2 ), as the climatic effect most closely related to population growth potential; the colder the winter inhabited by a population, the lower its growth potential, a relationship presumably molded by natural selection. By splitting the data into groups based on population MINDD01/2 and using a function suited to skewed normal distributions, regressions were developed for predicting growth from the distance in climate space (MINDD01/2 ) populations had been transferred from their native location to a planting site. The regressions were skewed, showing that the ecological optimum of most populations is colder than the physiological optimum and that the discrepancy between the two increases as the ecological optimum becomes colder. Response to climate change is dependent on innate growth potential and the discrepancy between the two optima and, therefore, is population-specific, developing out of genotype-environment interactions. Response to warming in the short-term can be either positive or negative, but long term responses will be negative for all populations, with the timing of the demise dependent on the amount of skew. The results pertain to physiological modeling, species distribution models, and climate-change adaptation strategies.

A haplotype-resolved chromosome-scale genome for Quercus rubra L. provides insights into the genetics of adaptive traits for red oak species.

Northern red oak (Quercus rubra L.) is an ecologically and economically important forest tree native to North America. We present a chromosome-scale genome of Q. rubra generated by the combination of PacBio sequences and chromatin conformation capture (Hi-C) scaffolding. This is the first reference genome from the red oak clade (section Lobatae). The Q. rubra assembly spans 739 Mb with 95.27% of the genome in 12 chromosomes and 33,333 protein-coding genes. Comparisons to the genomes of Quercus lobata and Quercus mongolica revealed high collinearity, with intrachromosomal structural variants present. Orthologous gene family analysis with other tree species revealed that gene families associated with defense response were expanding and contracting simultaneously across the Q. rubra genome. Quercus rubra had the most CC-NBS-LRR and TIR-NBS-LRR resistance genes out of the 9 species analyzed. Terpene synthase gene family comparisons further reveal tandem gene duplications in TPS-b subfamily, similar to Quercus robur. Phylogenetic analysis also identified 4 subfamilies of the IGT/LAZY gene family in Q. rubra important for plant structure. Single major QTL regions were identified for vegetative bud break and marcescence, which contain candidate genes for further research, including a putative ortholog of the circadian clock constituent cryptochrome (CRY2) and 8 tandemly duplicated genes for serine protease inhibitors, respectively. Genome-environment associations across natural populations identified candidate abiotic stress tolerance genes and predicted performance in a common garden. This high-quality red oak genome represents an essential resource to the oak genomic community, which will expedite comparative genomics and biological studies in Quercus species.

Height-growth response to climatic changes differs among populations of Douglas-fir: a novel analysis of historic data.

Projected climate change will affect existing forests, as substantial changes are predicted to occur during their life spans. Species that have ample intraspecific genetic differentiation, such as Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco), are expected to display population-specific growth responses to climate change. Using a mixed-effects modeling approach, we describe three-year height (HT) growth response to changes in climate of interior Douglas-fir populations. We incorporate climate information at the population level, yielding a model that is specific to both species and population. We use data from provenance tests from previous studies that comprised 236 populations from Idaho, Montana, and eastern Washington, USA. The most sensitive indicator of climate was the mean temperature of the coldest month. Population maximum HT and HT growth response to changes in climate were dependent on seed source climate. All populations had optimum HT growth when transferred to climates with warmer winters; those originating in sites with the warmest winters were taller across sites and had highest HT growth at transfer distances closest to zero; those from colder climates were shortest and had optimum HT growth when transferred the farthest. Although this differential response damped the height growth differences among populations, cold-climate populations still achieved their maximum growth at lower temperatures than warm-climate populations. The results highlight the relevance of understanding climate change impacts at the population level, particularly in a species with ample genetic variation among populations.

Ecological genetics of Juglans nigra: Differences in early growth patterns of natural populations.

Many boreal and temperate forest tree species distributed across large geographic ranges are composed of populations adapted to the climate they inhabit. Forestry provenance studies and common gardens provide evidence of local adaptation to climate when associations between fitness traits and the populations' home climates are observed. Most studies that evaluate tree height as a fitness trait do so at a specific point in time. In this study, we elucidate differences in early growth patterns in black walnut (Juglans nigra L.) populations by modeling height growth from seed up to age 11. The data comprise tree height measurements between ages 2 and 11 for 52 natural populations of black walnut collected through its geographic range and planted in one or more of 3 common gardens. We use the Chapman-Richards growth model in a mixed effects framework and test whether populations differ in growth patterns by incorporating populations' home climate into the model. In addition, we evaluate differences in populations' absolute growth and relative growth based on the fitted model. Models indicated that populations from warmer climates had the highest cumulative growth through time, with differences in average tree height between populations from home climates with a mean annual temperature (MAT) of 13°C and of 7°C estimated to be as high as 80% at age 3. Populations from warmer climates were also estimated to have higher and earlier maximum absolute growth rate than populations from colder climates. In addition, populations from warm climates were predicted to have higher relative growth rates at any given tree size. Results indicate that natural selection may shape early growth patterns of populations within a tree species, suggesting that fast early growth rates are likely selected for in relatively mild environments where competition rather than tolerance to environmental stressors becomes the dominant selection pressure.