Plasticity and the adaptive evolution of switchlike reaction norms under environmental change

Phenotypic plasticity is often posited as an avenue for adaptation to environmental change, whereby environmental influences on phenotypes could shift trait expression toward new optimal values. Conversely, plastic trait expression may inhibit adaptation to environmental change by reducing selective pressure on ill-adapted traits. While plastic responses are often assumed to be linear, nonlinear phenotype-environment relationships are common, especially in thermally sensitive traits. Here we examine nonlinear plasticity in a trait with great ecological and evolutionary significance: sexual phenotype in species with environmental sex determination (ESD). In species with ESD, development switches between male and female at an environmental threshold (the inflection point). The inflection point is a key trait for adaptive responses to changing environments and should evolve toward the new optimum in order to maintain evolutionarily stable sex ratios. We used an individual-based theoretical model to investigate how two forms of plasticity in the ESD reaction norm-the nonlinear slope of the reaction norm and a linear shift in the inflection point-influence the evolution of the inflection point under climate warming. We found that steeper reaction norm slopes (high nonlinear plasticity) promoted evolution toward new optimal phenotypes (higher inflection points). In contrast, increased linear plasticity in the inflection point (shift) hindered adaptive evolution. Additionally, populations in moderate warming scenarios showed greater adaptive evolution of the inflection point compared with populations in extreme warming scenarios, suggesting that the proximity of existing phenotypes to new optimal phenotypes influences evolutionary outcomes. Unexpectedly, we found greater population persistence under high climate variability, due to the increased production of rare-sex individuals in unusually cold years. Our results demonstrate that different forms of phenotypic plasticity have crucially different effects on adaptive evolution. Plasticity that prevented sex ratio bias hindered the evolution of the inflection point, while plasticity that exacerbated sex ratio bias promoted adaptation to environmental change. Trait variation in response to the environment, known as phenotypic plasticity, is common among living organisms and likely contributes to survival in variable environments. However, little is known about how plasticity in response to environmental upheaval, such as that caused by anthropogenic climate change, could influence evolution in the long term. This is especially true of traits where the relationship between phenotype and environment is not linear, that is, a change in environment does not result in a proportional trait change. We created a computer simulation to examine differences in how linear and nonlinear plasticity influence the evolution of plastic traits in a changing environment. We used an ecologically important plastic trait-sex (male/female) in species with environmental sex determination (ESD)-as a model for our investigation. Many reptiles, fish, and invertebrates display ESD, and while this form of sex determination can be advantageous, environmental change could put these species at risk. We found that nonlinear and linear plasticity can have different effects on adaptation to novel environments. The range of phenotypes that a trait with nonlinear plasticity can produce changes across environments, and as a result, nonlinear plasticity that provides a benefit in a species' normal range can become disadvantageous in an extreme environment. In contrast, in traits with linear plasticity, phenotype varies consistently with the environment, making changes in fitness outcome less likely. In our simulation, these differences led nonlinear plasticity to increase sex ratio bias in extreme environments, promoting the adaptive evolution of ESD. Linear plasticity balanced sex ratios, which hindered adaptation. This is an important result in understanding evolutionary responses to climate change, as many thermally sensitive traits have nonlinear relationships with temperature. Additionally, rising temperatures could reveal new nonlinear plasticity, as linear trait-environment relationships become less consistent under extreme conditions.