Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature

Experimentally transplanting guppies to evolve in a novel, predator-free environment reveals that the direction of plasticity in gene expression is usually opposite to the direction of adaptive evolution; that is, those genes whose expression changes are disadvantageous are more strongly selected upon than those whose changes are advantageous. Effect of phenotypic plasticity on selection Phenotypic plasticity may have a role in the evolutionary adaptation of populations to changed environmental conditions, but it has not been clear whether it facilitates or hinders adaptation. These authors allow guppies to evolve in a novel predator-free environment and look at the resulting changes in gene expression. They see that the genes that evolve expression differences are not those that were adaptively phenotypically plastic, but those whose plasticity of gene expression was non-adaptive in the ancestral population. In other words, genes whose expression reacts to the environment in an advantageous way tend not to evolve in response to selection, whereas those whose expression changes are disadvantageous are strongly selected on. Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation 1 . Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum 2 , 3 , 4 . Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 . Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies ( Poecilia reticulata ) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression