Plasticity via feedback reduces the cost of developmental instability

Costs of plasticity are thought to have important physiological and evolutionary consequences. A commonly predicted cost to plasticity is that plastic genotypes are likely to suffer from developmental instability. Adaptive plasticity requires that the developing organism can in some way sense what environment it is in or how well it is performing in that environment. These two information pathways—an “environmental signal” or a “performance signal” that indicates how well a developing phenotype matches the optimum in the current environment—can differ in their consequences for the organism and its evolution. Here, we consider how developmental instability might emerge as a side‐effect of these two distinct mechanisms. Because a performance cue allows a regulatory feedback loop connecting a trait to a feedback signal, we hypothesized that plastic genotypes using a performance signal would be more developmentally robust compared to those using a purely environmental signal. Using a numerical model of a network of gene interactions, we show that plasticity comes at a cost of developmental instability when the plastic response is mediated via an environmental signal, but not when it is mediated via a performance signal. We also show that a performance signal mechanism can evolve even in a constant environment, leading to genotypes preadapted for plasticity to novel environments even in populations without a history of environmental heterogeneity.