Ecological Genomics In Postglacial Fishes: The Gene Proposes and The Environment Disposes

Explaining the degree to which genetic variation can be explained by adaptive evolution remains a fundamental challenge in ecological genomics. Transition of an evolving population to a new adaptive optimum is predicted to leave a signature in the distribution of effect sizes of fixed mutations. Yet, phenotypic plasticity may also play an important role in adaptation by permitting population persistence in the face of novel environmental stressors, and subsequently evolving to increase fitness. Empirical evidence regarding the role of these processes during the colonization of novel environments is lacking. Here, data from two experiments in marine and derived freshwater populations of threespine stickleback (Gasterosteus aculeatus) demonstrate that a higher frequency of large effect genetic changes contributes to adaptive evolution in populations that adapt to a more distant optimum than to environments in which the optimum phenotype is nearer to the ancestral state. Pleiotropy, not just optimum overshoot, contributes to this difference. Genome-wide transcript abundance further supports a role for phenotypic plasticity in response to temperature change in these same populations, with derived populations exhibiting significantly more plastic transcripts, providing compelling evidence for the role of plasticity in population persistence and adaptation to temperature in freshwater environments. Collectively, these data support the notion that the gene proposes while the environment disposes during adaptive evolution to environnmental change.