Pre-adaptation to climate change through topography-driven evolution of traits and their plasticity

ABSTRACT Climate change is expected to increase the level of drought stress experienced by many plant populations, yet the spatial distribution of changes in dryness remains highly uncertain. Species can, to some extent, adapt to climate uncertainty through evolving increased trait plasticity. Biodiversity conservation could capitalize on such natural variation in the ability of populations to cope with climate variability. Yet, disentangling evolution of trait means vs. trait plasticity is challenging, as it requires a sampling design with genetic replicates grown under distinct environmental conditions. Here, we applied different soil moisture treatments to clones of Fragaria vesca plants that were raised from seeds that were sampled in distinct mountainous topographical settings, to study adaptive trait and plasticity divergence in response to drought. We demonstrate that various fitness traits evolved along topographical gradients, including increased specific leaf area (SLA) with increasing slope, and increased growth plasticity with increasing altitude. Our results indicate that traits and their plasticity can evolve independently in response to distinct topographical stressors. We further show that trait heritability varies considerably among traits and topographical settings. Heritability of phenotypic plasticity tended to increase with altitude for all traits, with populations from high altitudes harboring more than twice the heritability for growth and SLA plasticity compared to populations from low altitudes. We conclude that (i) low altitudinal populations, which are expected to be least vulnerable to climate change, may only withstand limited increases in drought stress, while (ii) populations that evolved to thrive under more heterogeneous mountain conditions are pre-adapted to climate change through high plasticity and heritability. Highly heterogeneous landscapes may thus represent invaluable sources of quantitative genetic variation that could support conservation under climate change across the globe.