Predicting the evolutionary dynamics of seasonal adaptation to novel climates in Arabidopsis thaliana
Significance Anticipating the effect of climate change on plants requires understanding its evolutionary consequence on traits and genes in complex realistic environments. How seasonal variation has an impact on the dynamics of adaptation in natural populations remains unclear. We simulated adaptation to different climate change scenarios, grounding our analysis in experimental data and explicitly exploring seasonal variation. Seasonal variation dramatically affected the dynamics of adaptation: Marked seasonality led to genetic differentiation within the population to different seasonal periods, whereas low seasonality led to a single population with fast evolving fitness. Our results suggest the prevalence of phenotypic plasticity across environmental conditions in determining how climate change will shift selection on traits and loci. In this unpredictable context, maintaining broad genomic diversity is critical. Predicting whether and how populations will adapt to rapid climate change is a critical goal for evolutionary biology. To examine the genetic basis of fitness and predict adaptive evolution in novel climates with seasonal variation, we grew a diverse panel of the annual plant Arabidopsis thaliana (multiparent advanced generation intercross lines) in controlled conditions simulating four climates: a present day reference climate, an increased temperature climate, a winter warming only climate, and a poleward migration climate with increased photoperiod amplitude. In each climate, four successive seasonal cohorts experienced dynamic daily temperature and photoperiod variation over a year. We measured 12 traits and developed a genomic prediction model for fitness evolution in each seasonal environment. This model was used to simulate evolutionary trajectories of the base population over 50 y in each climate, as well as 100 y scenarios of gradual climate change following adaptation to a reference climate. Patterns of plastic and evolutionary fitness response varied across seasons and climates. The increased temperature climate promoted genetic divergence of subpopulations across seasons, whereas in the winter warming and poleward migration climates, seasonal genetic differentiation was reduced. In silico "resurrection experiments" showed limited evolutionary rescue compared with the plastic response of fitness to seasonal climate change. The genetic basis of adaptation and, consequently, the dynamics of evolutionary change differed qualitatively among scenarios. Populations with fewer founding genotypes and populations with genetic diversity reduced by prior selection adapted less well to novel conditions, demonstrating that adaptation to rapid climate change requires the maintenance of sufficient standing variation.
Proceedings of the National Academy of Sciences