Genetic assimilation of ancestral plasticity during parallel adaptation

Abstract

Phenotypic plasticity in ancestral populations is hypothesised to facilitate adaptation, but evidence supporting its contribution is piecemeal and often contradictory. Further, whether ancestral plasticity increases the probability of parallel genetic and phenotypic adaptive changes has not been explored. The most general finding is that nearly all ancestral gene expression plasticity is reversed following adaptation, but this is usually examined transcriptome-wide rather than focused on the genes directly involved in adaptation. We investigated the contribution of ancestral plasticity to adaptive evolution of gene expression in two independently evolved lineages of zinc-tolerant Silene uniflora. We found that the general pattern of reversion is driven by the absence of a widespread stress response in zinc-adapted plants compared to ancestral, zinc-sensitive plants. Our experiments show that reinforcement of ancestral plasticity plays an influential role in the evolution of plasticity in derived populations and, surprisingly, one third of constitutive differences between ecotypes are the result of genetic assimilation of ancestral plasticity. Ancestral plasticity also increases the chance that genes are recruited repeatedly during adaptation. However, despite a high degree of convergence in gene expression levels between independently adapted lineages, genes with ancestral plasticity are as likely to have similar expression levels in adapted populations as genes without. Overall, these results demonstrate that ancestral plasticity does play an important role in adaptive parallel evolution, particularly via genetic assimilation across evolutionary replicates.