Understanding the influence of intraspecific genetic variation on the response of tree species to stress events—like heatwaves, droughts, and growing season frost—is crucial. This genetic variation is linked to species adaptive potential and plays a pivotal role in shaping the resilience and long-term adaptability of species to climate change. Furthermore, genetic variation can affect populations’ responses to stress events, thereby influencing forest productivity and carbon sequestration potential. We combined dendroecological and genomic approaches to analyze the growth response of 61 black spruce (Picea mariana) populations, grown for over 40 years in four common gardens, to daily extreme vapor pressure, soil moisture deficits, and growing season frosts. Our objectives were to 1) assess the effects of stress events defined from physiological thresholds on annual biomass production and 2) explore the potential influence of standing genetic variation on trees’ responses to stress events at the population scale. The growth response of black spruce to those events was site-specific but with an important influence of soil or atmospheric drought at most sites. This response was also nonlinear, with a negative effect on growth occurring only after several stress events a year. Additionally, an interaction between this response and the geographic origin of the population indicated an influence of standing genetic variation, notably linked to local adaptation. These results may provide insight into tree resilience to stress events and help estimate the adaptive potential of the Canadian boreal forest. Moreover, this knowledge can help guiding forest management, for example assisted gene flow.

Abstract Climate change (CC) necessitates reforestation/afforestation programs to mitigate its impacts and maximize carbon sequestration. But comprehending how tree growth, a proxy for fitness and resilience, responds to CC is critical to maximize these programs' effectiveness. Variability in tree response to CC across populations can notably be influenced by the standing genetic variation encompassing both neutral and adaptive genetic diversity. Here, a framework is proposed to assess tree growth potential at the population scale while accounting for standing genetic variation. We applied this framework to black spruce (BS, Picea mariana [Mill] B.S.P.), with the objectives to (1) determine the key climate variables having impacted BS growth response from 1974 to 2019, (2) examine the relative roles of local adaptation and the phylogeographic structure in this response, and (3) project BS growth under two Shared Socioeconomic Pathways while taking standing genetic variation into account. We modeled growth using a machine learning algorithm trained with dendroecological and genetic data obtained from over 2600 trees (62 populations divided in three genetic clusters) in four 48-year-old common gardens, and simulated growth until year 2100 at the common garden locations. Our study revealed that high summer and autumn temperatures negatively impacted BS growth. As a consequence of warming, this species is projected to experience a decline in growth by the end of the century, suggesting maladaptation to anticipated CC and a potential threat to its carbon sequestration capacity. This being said, we observed a clear difference in response to CC within and among genetic clusters, with the western cluster being more impacted than the central and eastern clusters. Our results show that intraspecific genetic variation, notably associated with the phylogeographic structure, must be considered when estimating the response of widespread species to CC.