Genome-wide evolutionary response of European oaks during the Anthropocene.

The pace of tree microevolution during Anthropocene warming is largely unknown. We used a retrospective approach to monitor genomic changes in oak trees since the Little Ice Age (LIA). Allelic frequency changes were assessed from whole-genome pooled sequences for four age-structured cohorts of sessile oak (Quercus petraea) dating back to 1680, in each of three different oak forests in France. The genetic covariances of allelic frequency changes increased between successive time periods, highlighting genome-wide effects of linked selection. We found imprints of parallel linked selection in the three forests during the late LIA, and a shift of selection during more recent time periods of the Anthropocene. The changes in allelic covariances within and between forests mirrored the documented changes in the occurrence of extreme events (droughts and frosts) over the last 300 years. The genomic regions with the highest covariances were enriched in genes involved in plant responses to pathogens and abiotic stresses (temperature and drought). These responses are consistent with the reported sequence of frost (or drought) and disease damage ultimately leading to the oak dieback after extreme events. They provide support for adaptive evolution of long-lived species during recent climatic changes. Although we acknowledge that other sources (e.g., gene flow, generation overlap) may have contributed to temporal covariances of allelic frequency changes, the consistent and correlated response across the three forests lends support to the existence of a systematic driving force such as natural selection.

How does contemporary selection shape oak phenotypes?

Most existing forests are subjected to natural and human-mediated selection pressures, which have increased due to climate change and the increasing needs of human societies for wood, fibre and fuel resources. It remains largely unknown how these pressures trigger evolutionary changes. We address this issue here for temperate European oaks (Quercus petraea and Q. robur), which grow in mixed stands, under even-aged management regimes. We screened numerous functional traits for univariate selection gradients and for expected and observed genetic changes over two successive generations. In both species, growth, leaf morphology and physiology, and defence-related traits displayed significant selection gradients and predicted shifts, whereas phenology, water metabolism, structure and resilience-related traits did not. However, the direction of the selection response and the potential for adaptive evolution differed between the two species. Quercus petraea had a much larger phenotypic and genetic variance of fitness than Q. robur. This difference raises concerns about the adaptive response of Q. robur to contemporary selection pressures. Our investigations suggest that Q. robur will probably decline steadily, particularly in mixed stands with Q. petraea, consistent with the contrasting demographic dynamics of the two species.

Heritability and genetic architecture of reproduction-related traits in a temperate oak species.

Reproduction, one of the main components of plant fitness, is highly variable in response to environmental cues, but little is known about the genetic determinism underlying reproduction-related traits in forest tree species. There is therefore an urgent need to characterize the genetic architecture of those traits if we are to predict the evolutionary trajectories of forest populations facing rapidly changing environment and mitigate their impacts. Using a full-sib family of pedunculate oak (Quercus robur), we investigated the within population variability of seed production and mean seed mass during four consecutive years. Reproductive traits were highly variable between trees and between years. The high narrow sense heritability and evolvability estimated underline the important genetic effect on the variability in seed production and mean seed mass. Despite a large variability over years, reproductive traits show significant genetic correlation between years. Furthermore, for the first time in forest tree species, quantitative trait loci (QTLs) associated with seed production and mean mass of a seed have been identified. While it is commonly assumed and observed that fitness-traits have low narrow sense heritabilities, our findings show that reproduction-related traits may undergo evolutionary changes under selective pressure and may be determinant for tree adaptation.