The influence of post-glacial migration and hybridization on the gene pool of marginal Quercus pubescens populations in Central Europe

Abstract

Background and aims: In Central Europe, the drought-tolerant downy oak (Quercus pubescens) is at the northern edge of its natural distribution range, often growing in small and spatially isolated populations. Here, we elucidate how the population genetic structure of Central European Q. pubescens was shaped by geographical barriers, genetic drift and introgression with the closely related sessile oak (Q. petraea).

Methods: In total, 27 Q. pubescens populations from the northern margin of its natural distribution range were sampled. Based on 16 nuclear microsatellite markers (nSSRs), Bayesian clustering and distance-based analyses were performed to determine the intraspecific genetic structure and to identify genetic barriers. To identify drivers of introgression with Q. petraea, generalized linear models were applied to link levels of introgression with environmental conditions. To track post-glacial migration routes, the spatial distribution of haplotypes based on eight chloroplast microsatellite markers (cpSSRs) was investigated.

Key results: Based on nSSRs, the study populations of Q. pubescens were divided into a western and an eastern genetic cluster. Within these clusters, more pronounced genetic substructure was observed in the west, probably due to a rugged topography and limited gene flow. Introgression from Q. petraea was more prevalent at wetter and north-exposed sites and in the west. The identified cpSSR haplotypes followed known migration pathways.

Conclusions: Our results suggest two late-glacial refugia in or near the southwestern Alps and the southeastern Alps as potential sources for post-glacial migration. Although some genetic exchange is evident in northern Italy, south of the Alps, the two clusters remain distinct at a large scale. Landscape features and introgression with Q. petraea shaped the genetic substructure at a smaller scale. Our study provides a comprehensive overview of the genetic structure of Q. pubescens in Central Europe, relevant for conservation.

Keywords: Quercus pubescens; downy oak; genetic differentiation; genetic diversity; haplotype; hybridization; introgression; microsatellites; peripheral populations; short sequence repeats; white oaks.

Fig. 1.

Study area and examined populations. The natural distribution range (Caudullo et al., 2024) of Quercus pubescens is illustrated in green. The locations of the studied downy oak populations are shown with black dots. Population IDs are indicated in the enlarged map.

Fig. 2.

Species identification: Structure barplot with 27 putative Q. pubescens populations, four Q. petraea populations and four Q. robur populations (K = 4). Each box represents a study population, each bar within a box illustrates an individual while the inferred clusters are shown with different colours.

Fig. 3.

Principal coordinate analysis (PCoA) of all studied Q. pubescens populations (only pure individuals) and Q. petraea and Q. robur reference populations based on pairwise F_ST values after Nei (1987) (for values see Supplementary Data Table S8).

Fig. 4.

Population genetic structure of Q. pubescens. Each population is represented by a pie chart and the colours indicate the membership proportion for each genetic cluster inferred by Structure. (A) K = 2 for all pure Q. pubescens; (B) K = 5 for Eastern populations; (C) K = 6 for Western populations.

Fig. 5.

Gene flow barriers among Q. pubescens populations. The eight selected barriers (a–h) are shown with orange or red lines (different colours are used just for visualization). The beginning of a barrier is marked by the letters a–h and the end by aʹ–hʹ. Beside each segment of a barrier line is a number which indicates the bootstrap value.

Fig. 6.

Minimum spanning network (at the top) of cpSSR haplotypes. Vertical lines represent missing haplotypes. Reference haplotypes from refugial areas (Neophytou and Michiels, 2013) were used to construct the minimum spanning network (colourless circles). Haplotypes found in this study are indicated with different colours. The size of the circle reflects the frequency of the haplotypes. Map (at the bottom) with pie charts showing the different haplotypes within different populations.

Fig. 7.

Effect of environmental descriptors on introgression index of Q. pubescens populations. Shown are the descriptors and their coefficients (error bars: 95% confidence intervals) included in the best model (generalized R² = 0.59) resulting from the model selection procedure (*P < 0.05, **P < 0.01 and ***P < 0.001).