Fluctuating selection and rapid evolution of oaks during recent climatic transitions

Societal Impact Statement The rapidity of evolutionary changes in trees and whether this pace is sufficient to cope with ongoing climatic change are hotly debated issues in ecology today. Climate warming began in the mid‐19th century, after the Little Ice Age (LIA). Monitoring temporal genetic changes during this climatic transition in multicentennial oak populations revealed evidence of fluctuating selection and rapid evolution. These findings suggest that rapid evolution is probably also currently underway. They may lead to management options for operational forestry aiming to stimulate evolutionary mechanisms during the renewal of oak stands and to decrease potential temporal gene flow. Summary Retrospective studies of the evolutionary responses of tree populations to past documented climate change can provide insight into the adaptive responses of these organisms to ongoing environmental changes. We used a retrospective approach to monitor genetic changes over time in multicentennial sessile oak (Quercus petraea L.) forests. We compared the offspring of three age‐structured cohorts (340, 170, and 60 years old, dating from about 1680, 1850, and 1960) spanning the late Little Ice Age and early Anthropocene. The experiment was repeated in three different forests in western France. The offspring were raised in a common garden experiment, with 30 to 53 open‐pollinated families per cohort. We assessed 16 phenotypic traits in the common garden and observed significant shifts between cohorts for growth and phenology‐related traits. These shifts were correlated with differences in the prevailing temperatures in the past and could be interpreted as temporal genetic changes. However, there was no temporal trend for genetic variation. The genetic changes between the cold (late Little Ice Age) and warm (early Anthropocene) periods were mostly opposite for growth and phenology‐related traits. These findings highlight fluctuations of selection and a rapid evolutionary response of tree populations to climatic transitions in the past, suggesting that similar trends may be at work now. We discuss these results in terms of the mode and direction of evolution, and their potential implications for the adaptive management of oak forests. La vitesse d'évolution des arbres et leur capacité à répondre au changement climatique sont très largement débattues aujourd'hui en écologie et en biologie évolutive. Dans cet article les auteurs ont mesuré les changements génétiques sur de