Rapid evolutionary adaptation: Potential and constraints

The vast diversity of life on earth is the result of evolutionary pro-cesses that acted over billions of years. Historically it was assumed that adaptation and the origin of new species required long periods of time. However, it is now well established that adaptation to new environments can occur rapidly and sometimes even within a few generations. We define here rapid adaptation as a selective process, which allows a population or species to substantially improve its average fitness in the short time scale of few tens of generations, typically within a hundred years for annual species. More precisely, rapid adaptation occurs through natural selection acting on the phenotype (and ultimately on the underlying genetic variants) over short time scale and therefore encompasses both ecological (demographic abundance and inter-specific interactions within a given habitat and species community) and evolutionary (genetic drift, mutation, recombination, gene flow and selection) processes (Hairston et al., 2005; Kokko et al., 2017). The occurrence and speed of rapid adaptation is thus determined by the feedback between ecological and evolutionary (eco-evo) processes. A large body of literature now documents examples of eco-evo feedbacks driving rapid adaptation especially as consequences of human activities, with damaging consequences in agriculture (e.g. invasion of crop pests and pathogens resistant to fungicides) (Fisher et al., 2022), medicine (e.g. parasite resistance to drugs/antibiotics) (Birkholtz et al., 2022; Zhang et al., 2022) and/or ecosystems (e.g. new invasive species and emergent diseases) (Fisher et al., 2012). Indeed, rapid adaptation underpins species' invasion of new habitats, coevolution between hosts and their parasites, fluctuating selection due to fast environmental change or adaptation to human-altered environments. Deciphering the evolutionary mechanisms of rapid adaptation is thus critical given the current rate of global change and loss of biodiversity to forecast the evolutionary potential of species and promote ad hoc conservation measures and/or to prevent the emergence of novel and unwanted pathogens. This research endeavour entails two major questions bridging eco-logical and evolutionary processes and mechanisms: What are the sources of genetic variation for rapid evolution? Which evolutionary, ecological and genetic factors enable (hasten) and which factors constrain (slow down) rapid evolution?