Plastic responses to past environments shape adaptation to novel selection pressures

Abstract

Phenotypic plasticity may pave the way for rapid adaptation to newly encountered environments. Although it is often contested, there is growing evidence that initial plastic responses of ancestral populations to new environmental cues may promote subsequent adaptation. However, we do not know whether plasticity to cues present in the ancestral habitat (past-cue plasticity) can facilitate adaptation to novel cues. Conceivably, this could occur if plastic responses are coincidentally optimal to both past and novel cues (i.e., are pre-adaptive) or if they are transferred to novel cues during adaptation. Past plastic phenotype values could also become fixed and genetically co-opted during adaptation to the new environment. To uncover the role of past-cue plasticity in adaptation, we tested gene expression plasticity responses of two parallel mine-waste adapted Silene uniflora populations and their closest coastal relatives. Plants were exposed to the past and novel-cues of salt and zinc, which revealed that during adaptation to mine-waste plasticity to salt diminishes. Despite this, our results show that ancestral plasticity to salt has a substantial impact on subsequent adaptation to zinc. For a third of genes that have evolved zinc plasticity in mine populations, salt plasticity has been transferred to the zinc response. Furthermore, a quarter of fixed expression differences between mine and coastal populations were similar to ancestral salt responses. Alongside evidence that ancestral plasticity to novel cues can facilitate adaptation, our results provide a clear indication that ancestral past-cue plasticity can also play a key role in rapid, parallel adaptation to novel habitats. Significance StatementThe role of phenotypic plasticity in promoting adaptation is hotly debated, with conflicting evidence for the benefits of ancestral plasticity in newly encountered environments. Here, we present an alternative mode by which ancestral plasticity can promote adaptation. We investigated whether phenotypic plasticity towards environmental cues that are experienced only in ancestral habitats (past-cue plasticity) can significantly contribute towards rapid adaptation to completely distinct cues. We show that, in the maritime plant species, Silene uniflora, past-cue plasticity to salt has made a substantial contribution to rapid adaptation to heavy-metal pollution in newly encountered habitats. This phenomenon has broad implications for the capacity and predictability of species to persist in the face of anthropogenic environmental change.