Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity

Abstract

Adaptive phenotypic plasticity allows organisms to cope with environmental variability, and yet, despite its adaptive significance, phenotypic plasticity is neither ubiquitous nor infinite. In this review, we merge developmental and population genetic perspectives to explore costs and limits on the evolution of plasticity. Specifically, we focus on the role of modularity in developmental genetic networks as a mechanism underlying phenotypic plasticity, and apply to it lessons learned from population genetic theory on the interplay between relaxed selection and mutation accumulation. We argue that the environmental specificity of gene expression and the associated reduction in pleiotropic constraints drive a fundamental tradeoff between the range of plasticity that can be accommodated and mutation accumulation in alternative developmental networks. This tradeoff has broad implications for understanding the origin and maintenance of plasticity and may contribute to a better understanding of the role of plasticity in the origin, diversification, and loss of phenotypic diversity.

Figure 1

Conditions under which relaxed selection may limit the origin and maintenance of plasticity. In this figure, individuals are represented as outlined boxes, genes as lower-case letters, and environments as shaded boxes. (A): Relaxed selection may constrain the evolution of plasticity when environment-specific traits are associated with environment-specific expression of genes and individuals experience environmental variation in a coarse-grained manner. Relaxed selection will not constrain the evolution of plasticity when (B) environment-specific traits develop through mechanisms that do not require environment-specific gene expression (e.g., “hypervariable plasticity”), and (C) individuals experience environmental variation in a fine-grained manner and plastic traits are reversible.