The evolution of freezing tolerance in oaks

Abstract

Freezing tolerance is a critical factor controlling the broad-scale distribution of organisms. Freezing temperatures result in intra- and extracellular ice crystal formation, which can cause physical damage and cellular dehydration, resulting in losses of xylem function. Yet, how rapidly plants can adapt to changing climate and whether there are trade-offs between freezing tolerance and growth remain poorly understood. We grew 48 species of Quercus (oaks) from five sections of the genus under temperate and tropical growth conditions and measured their stem freezing tolerance and growth rate. We found significant differences among species in their freezing tolerance and their capacity to cold acclimate. Species from colder regions have higher freezing tolerance and slower growth rates than species from warmer climates. Nevertheless, a direct evolutionary trade-off did not emerge because deciduousness rather than freezing tolerance appears to constrain growth rates. Deciduous species have consistently slower growth rates than evergreen species regardless of climatic niche but vary markedly in freezing tolerance in step with the broad climatic range they span. In contrast, evergreen species occur only in warm climates and have low freezing tolerance. Species from colder regions also have higher acclimation potential than species from warmer areas, indicating that cold-climate species have evolved higher capacity to acclimate to seasonal fluctuations in climate, while warm-climate species have constraints to surviving in colder climates. Freezing tolerance in the oaks is relatively close to its optimal evolutionary state (r=0.77), however, the phylogenetic half-life is 8.9 Myr (ca. 17% of the crown age of the genus). Consequently, despite a high level of adaptation to the climates in which species occur, evolution towards optimal freezing tolerance has a considerable lag time.