Fine-Scale Variation in Soil Properties Promotes Local Taxonomic Diversity of Hybridizing Oak Species (Quercus spp.)

Abstract

Although many tree species frequently hybridize and backcross, management decisions in forestry and nature conservation are usually concentrated on pure species. Therefore, understanding which environmental factors drive the distribution and admixture of tree species on a local stand scale is of great interest to support decision-making in the establishment and management of resilient forests. Here, we extensively sampled a mixed stand of hybridizing white oaks (Quercus petraea and Q. pubescens) near Lake Neuchâtel (Switzerland), where limestone and glacier moraine geologies coexist in proximity, to test whether micro-environmental conditions can predict taxonomic distribution and genetic admixture. We collected DNA from bud tissue, individual soil samples, and extracted high-resolution topographic data for 385 oak trees. We used 50 species-discriminatory single nucleotide polymorphism (SNP) markers to determine the taxonomic composition and admixture levels of individual trees and tested their association with micro-environmental conditions. We show that the trees' taxonomic distribution can be explained mainly by geographic position, soil pH, and potential rooting depth, a proxy for soil water availability. We found that admixed individuals tend to grow in habitats that are characteristic of the more drought-tolerant species Q. pubescens rather than in intermediate habitats. Using in situ measurements, we are the first to show that fine-scale variation in soil properties related to pH and water availability potentially drives the distribution of hybridizing tree species in a mixed stand. Microenvironmental variation therefore promotes local taxonomic diversity, facilitates admixture and adaptive introgression, and contributes to the resilience of forests under environmental change. Consequently, species such as white oaks should be managed and protected as a species complex rather than as pure species.

Keywords: Quercus; adaptation; drought; hybridization; oaks; soil.

FIGURE 1

Sampling site and study design. White circles indicate the position of the 385 sampled trees. Background aerial image from Swissimage (10 cm resolution, swisstopo).

FIGURE 2

Taxonomic assignment of the sampled trees. structure plot showing assignment probabilities for reference and test individuals to the three species Quercus petraea , Q. pubescens, and Q. robur . Samples were analyzed with 50 species‐diagnostic single‐nucleotide polymorphism (SNP) markers. Each bar represents a single tree, and the colors represent assignment probabilities for the respective species. Reference individuals (left, N = 194) are grouped by species. Test individuals (right, N = 380) are sorted from West to East.

FIGURE 3

Environmental variables with a significant effect on the taxonomic proportion of Quercus pubescens in individual trees. Significant environmental variables (see Table 1 for details) and their coefficients resulting from generalized linear models with assignment probabilities (Q‐values) of Q. pubescens as the response variable. Results are shown for the full (left figure) and reduced (right figure) sampling transects. The horizontal bars indicate the 95% confidence intervals as estimated from the models. R ²‐values indicate the explanatory power of each model. Significance levels are indicated as follows: *p < 0.05; **p < 0.01; ***p < 0.001. Points are sized according to the posterior model inclusion probability of each variable and colored according to their sign inferred from the Bayesian model averaging.

FIGURE 4

Partial redundancy analysis showing the contribution of environmental variables to the taxonomic variation of Quercus spp. while accounting for the effect of geographic position. Species are indicated in blue, and environmental variables (see Table 1 for details) in red. Arrows display the direction of effects of environmental variables on taxonomic variation. Arrow length shows the strength of the effect. Adjusted R ²‐values indicate the explanatory power of the model. The constrained variation explained by axis 1 (RDA1) and axis 2 (RDA2) is indicated in brackets.

FIGURE 5

Tree taxonomy on interpolated soil maps. Two maps displaying potential rooting depth (top) and soil pH (bottom) derived and interpolated from in situ measurements. Individual trees (circles) are colored according to Quercus pubescens Q‐values. Background aerial image from Swissimage (10 cm resolution, swisstopo).

FIGURE 6

Soil properties of pure and admixed individuals. Boxplots showing the distribution of potential rooting depth (top) and topsoil pH (bottom) grouped by taxonomic categories (pure Quercus petraea : Q‐value < 10%; admixed individuals: Q‐value = 10%–90%; pure Q. pubescens: Q‐value > 90%). Line plots on top of the boxplots indicate the variation (measured as standard deviation) for potential rooting depth (top) and topsoil pH (bottom). Significance levels of the Tukey's post hoc test between groups are indicated above the boxplots as follows: ^n.s. p > 0.05; *p < 0.05; **p < 0.01; ***p < 0.001.