Remodeling Ancestral Phenotypic Plasticity in Local Adaptation: A New Framework to Explore the Role of Genetic Compensation in the Evolution of Homeostasis

Phenotypic plasticity is not universally adaptive. In certain cases, plasticity can result in phenotypic shifts that reduce fitness relative to the un-induced state. A common cause of such maladaptive plasticity is the co-option of ancestral developmental and physiological response systems to meet novel challenges. Because these systems evolved to meet specific challenges in an ancestral environment (e.g., localized and transient hypoxia), their co-option to meet a similar, but novel, stressor (e.g., reductions in ambient pO(2) at high elevation) can lead to misdirected responses that reduce fitness. In such cases, natural selection should act to remodel phenotypic plasticity to suppress the expression of these maladaptive responses. Because these maladaptive responses reduce the fitness of colonizers in new environments, this remodeling of ancestral plasticity may be among the earliest steps in adaptive walks toward new local optima. Genetic compensation has been proposed as a general form of adaptive evolution that leads to the suppression of maladaptive plasticity to restore the ancestral trait value in the face of novel stimuli. Given their central role in the regulation of basic physiological functions, we argue that genetic compensation may often be achieved by modifications of homeostatic regulatory systems. We further suggest that genetic compensation to modify homeostatic systems can be achieved by two alternative strategies that differ in their mechanistic underpinnings; to our knowledge, these strategies have not been formally recognized by previous workers. We then consider how the mechanistic details of these alternative strategies may constrain their evolution. These considerations lead us to argue that genetic compensation is most likely to evolve by compensatory physiological changes that safeguard internal homeostatic conditions to prevent the expression of maladaptive portions of conserved reaction norms, rather than direct evolution of plasticity itself. Finally, we outline a simple experimental framework to test this hypothesis. Our goal is to stimulate research aimed at providing a deeper mechanistic understanding of whether and how phenotypic plasticity can be remodeled following environmental shifts that render ancestral responses maladaptive, an issue with increasing importance in our current era of rapid environmental change.