Range expansion can promote the evolution of plastic generalism in coarse-grained landscapes

Phenotypic plasticity is one way for organisms to deal with variable environments through generalism. However, plasticity is not found universally and its evolution may be constrained by costs and other limitations such as complexity: the need for multiple mutational steps before the adaptation is realized. Theory predicts that greater experienced heterogeneity, such as organisms may encounter when spatial heterogeneity is fine-grained relative to dispersal, should favor the evolution of a broader niche. Here we tested this prediction via simulation. We found that, contrary to classical predictions, coarse-grained landscapes can be the most favorable for the evolution of plasticity, but only when populations encounter those landscapes through range expansion. During these range expansions, coarse-grained landscapes select for each step in the complex mutational pathway to plastic generalism by blocking the dispersal of specialists. These circumstances provide ecological opportunities for innovative mutations that change the niche. Our results indicate a new mechanism by which range expansion and spatially structured landscapes interact to shape evolution and reveal that the environments in which a complex adaptation has the highest fitness may not be the most favorable for its evolution. What types of environments favor specialists and which drive the evolution of generalists? Intuitively, generalists should do best when landscapes are highly variable. However, in simulations we found that coarse-grained landscapes, featuring large clusters of each type of environment, could be the most favorable for the evolution of plastic generalists. This surprising result occurred in populations expanding into new areas: in this scenario, coarse-grained heterogeneity was both selected for generalists and impeded the movement of specialists. In this study, we show that barriers to the dispersal of specialists can reward mutations that change an organism's niche. This interaction of ecology and evolution drives the exploration of genotype space, rapidly producing the complex trait of plasticity. Our results point to surprising ways in which expanding populations experience selection differently from those that are stationary, potentially leading to innovative evolutionary outcomes. Organisms regularly encounter uncertainty and variety in the types of environments they encounter. Phenotypic plasticity, a strategy in which organisms produce different traits based on cues they receive from the environment, seems like an ideal solution to cope with this variation. Phenotypic plasticity is present in nature, but it is not ubiquitous, which points to the possibility that its evolution is constrained. One possible constraint is that multiple mutations might be required to produce a plastic organism. The waiting time to assemble these multiple mutations might be prohibitively long unless each one provides an immediate benefit to the individuals who carry it. Here we use computer simulations to look at how the evolution of plasticity plays out during range expansion events, in which a population enters a new area for the first time. We find that landscapes with large, clustered patches of each environment most readily promote the evolution of phenotypic plasticity during range expansions, because these large patches inhibit the movement of specialists that can only thrive in one environment. These results contradict older predictions with regard to which type of landscapes would be most favorable for the evolution of this complex trait and point us toward new complexities in the ways in which expanding populations adapt.