The Baldwin Effect Reloaded: Intermediate Levels of Phenotypic Plasticity Favor Evolutionary Rescue

AbstractSince the late 1890s up until today, how phenotypic plasticity interacts with genetic adaptation has been a debated issue. Proponents of a positive causal role of phenotypic plasticity-James M. Baldwin in the first place-supported the view that in altered environmental conditions, phenotypic plasticity is a key factor allowing a population to avoid extinction and then genetic evolution to catch up ("original Baldwin effect" [OBE]). Opponents, such as Ernst Mayr, regularly pointed out that phenotypic plasticity, by masking genetic variation, slows gene-level evolution ("Mayr effect" [ME]). For decades, this opposition remained only verbal and qualitative. To resolve it, we propose here a stochastic model that, following Baldwin's intuitive take, combines the minimal number of ingredients to account for extinction, selection, mutation, and plasticity. We study evolutionary rescue of the population (arrival and invasion of an adaptive genetic mutant) in the altered environment for different values of phenotypic plasticity, here quantified as the probability p that the maladapted genotype develops into the adapted phenotype. Our claim is that OBE can be a genuine evolutionary mechanism, depending on the level of phenotypic plasticity with respect to a threshold value p^⋆. When $p<p^{\star }$, increasing p promotes evolutionary rescue by delaying extinction ("strong" OBE); when $p>p^{\star }$, plasticity sustains population survival and increasing p has two antagonistic effects: to accelerate adaptation by increasing the supply of adaptive mutants ("weak" OBE, intermediate values of p) and to slow down adaptation by decreasing their fitness advantage (ME, high values of p).