Climate change intensifies rapid genomic selection beyond the ancestral niche of Fagus sylvatica

Abstract

As climate change accelerates, the persistence of long-lived organisms increasingly depends on their capacity to adapt in situ. While phenotypic plasticity provides an immediate buffer, it remains uncertain whether forest trees can evolve rapidly enough to track shifting climatic niches. Here, we investigate the adaptive potential of European beech (Fagus sylvatica L.), a keystone temperate species, by leveraging different growth classes as a quasi-time-series. This approach allows us to compare growth classes established under the relatively stable climate of the early 20th century against those regenerating under contemporary warming (+1.1{degrees}C global mean temperature increase). Integrating pool-seq data from three growth classes across 43 sites in Germany with satellite-derived environmental stress indicators, we characterised past, current and projected future climate-driven selection. We detected rapid, genome-wide selective sweeps between the oldest and youngest growth classes, particularly in sites already exceeding their historical climatic niche (defined as the 95% confidence interval of pre-warming conditions). Notably, selection signatures have shifted over time: while older classes show signatures related to biotic interactions, younger cohorts exhibit intense selection on genes managing abiotic heat and drought stress. In the warmest regions, we estimated exceptionally high selection coefficients (s{approx}2), suggesting intense selection where beech trees exceed their ancestral niche. In older growth classes, distance and geology account for genetic differences between populations but in young growth classes climate is the primary factor, highlighting the importance of climate change. However, predictive modelling reveals a critical threshold to this resilience. While adaptive potential appears sufficient to maintain population persistence under low-emission scenarios (SSP1-2.6), high-emission trajectories (SSP5-8.5) are projected to rapidly outpace the species evolutionary capacity. These findings demonstrate that while trees can undergo remarkably rapid genomic shifts, the sheer velocity of unmitigated climate change threatens to exceed the fundamental limits of forest adaptation.