Abstract

Aim

Knowledge of the distribution of genetic variation at the cold-limited range margin and its alignment with changing climate conditions is critical to understand future range dynamics and productivity patterns. Yet, for most tree species, such information is still lacking. To address this, we examined patterns of neutral and adaptive genetic variation at the northern range margin of the long-lived Quercus robur.

Location

Sweden

Methods

We RAD-seq genotyped oaks from 21 northern marginal stands across five latitudinal degrees, and examined the relationship between genetic variation and latitude (proximity to range margin) for neutral and adaptive variation. With outlier analysis and gene-environment associations, we investigated potential drivers of spatially varying selection and identified candidate genes. Finally, we estimated climate vulnerability (genomic offset) and evaluated its predictive capacity using performance data from common garden trials.

Results

Results revealed limited among-stand differentiation, suggesting that all stands belong to a single genetic cluster, and indicated maintained adaptive variation across the latitudinal gradient despite declining neutral variation. Results identified signatures of spatially varying selection and local adaptations, and suggested that environmental conditions (spring and fall frost - whose timing and severity change with global warming) and trophic interactions likely have shaped the genetic variation and structure. Climate vulnerability analysis pointed to stand-specific rather than spatial effects and indicated that genomic offset - performance associations were weak at best.

Main conclusion

Our findings underscore the need for management to consider adaptive (rather than neutral) genetic variation and to preserve the diversity of stand-specific adaptations. Securing the overall adaptive potential and portfolio effects may enable this keystone species to cope with rapidly changing and uncertain future environmental conditions, thereby safeguarding associated biodiversity. Finally, the findings complicate generalizations regarding climate-vulnerability and call into question the utility of genomic offset estimates to inform management strategies at this spatial scale.

Theory, manipulation experiments and observational studies on biodiversity and ecosystem functioning largely concur that higher intraspecific diversity may increase the overall productivity of populations, buffer against environmental change and stabilize long-term productivity. However, evidence comes primarily from small and short-lived organisms. We tested for effects of genetic diversity on variation in forest growth by combining long-term data on annual individual growth rate (basal area increment (BAI)) with estimates of intrapopulation genetic variation (based on RAD-seq SNPs) for 18 natural Quercus robur pedunculate oak populations. Higher total or adaptive genetic variability of populations was neither associated with faster average growth nor with increased temporal or spatial stability of growth nor with among-individual asynchrony in growth. However, as expected, we found that greater asynchrony of growth responses within the populations increased their temporal stability. Together, these findings point towards a negligible role of genetic variation in structuring growth patterns in natural populations of tree species. Identifying which environmental factors and phenotypic traits (and its genetic basis) contribute to asynchronous growth responses is an important next step towards a better mechanistic understanding of the causes of temporal stability in tree growth and forest productivity.

The genetic variability of plant populations can shape their disease resistance; additionally, plant pathogens commonly modify the fitness and distribution of co-occurring plant-feeding insects. Host genetics may therefore induce cascading effects mediated via tripartite interactions at the population level. However, whether the mechanisms connecting plant genetic variability to pathogen infection and its effect on the associated insect community structure are sufficiently strong to manifest in natural populations is unclear. Using Quercus robur oak populations in Sweden as a model system, we show that powdery mildew (Erysiphe alphitoides) pathogen infection levels were higher in oak populations with lower inter-individual genetic variability. In turn, higher infection levels were associated with an increasingly patchy distribution of the associated plant-feeding insects among trees within populations. Lastly, the occurrence of leaf miners and gallers decreased with increasing infection levels within trees, but this pattern was less evident among trees and non-existing among populations, indicating scale-dependence. These results support that high genetic variability among hosts improves disease resistance in forests, and suggest that, via modified disease levels, genetic variability may indirectly affect the structure of the insect community.

That genetically more diverse plant populations should host more diverse and abundant assemblages of associated species is well established in ecology. However, it remains unclear whether these effects are sufficiently strong to manifest in natural forest systems, whether different organism groups are differently impacted, and whether host genetic diversity is more or less important than other known biodiversity drivers. Using data from 17 forests, we show that oak populations with greater genetic diversity had higher species richness and abundance of specialist consumers (leaf miners and gallers), higher abundance of producers (epiphytic mosses), and lower community differences among trees for miners and gallers, and epiphytic lichens. Neither specialist nor generalist arthropods or vascular plants showed significant associations. When present, the contribution of genetic diversity was comparable to or greater than latitude and oak biomass. These taxon-specific responses have implications for the planning and assessment of forest management and biodiversity protection.