Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity

Abstract

Phenotypic plasticity is ubiquitous and generally regarded as a key mechanism for enabling organisms to survive in the face of environmental change. Because no organism is infinitely or ideally plastic, theory suggests that there must be limits (for example, the lack of ability to produce an optimal trait) to the evolution of phenotypic plasticity, or that plasticity may have inherent significant costs. Yet numerous experimental studies have not detected widespread costs. Explicitly differentiating plasticity costs from phenotype costs, we re-evaluate fundamental questions of the limits to the evolution of plasticity and of generalists vs specialists. We advocate for the view that relaxed selection and variable selection intensities are likely more important constraints to the evolution of plasticity than the costs of plasticity. Some forms of plasticity, such as learning, may be inherently costly. In addition, we examine opportunities to offset costs of phenotypes through ontogeny, amelioration of phenotypic costs across environments, and the condition-dependent hypothesis. We propose avenues of further inquiry in the limits of plasticity using new and classic methods of ecological parameterization, phylogenetics and omics in the context of answering questions on the constraints of plasticity. Given plasticity's key role in coping with environmental change, approaches spanning the spectrum from applied to basic will greatly enrich our understanding of the evolution of plasticity and resolve our understanding of limits.

Figure 1

Classic framework for evaluating cost of plasticity, and contrast with a cost of phenotype. In each environment (no predator vs predator), genotypes 1 (G1) and 2 (G2) differ in the phenotypes (200 vs 800 μm) they produce, leading to differences in fitness—these represent costs to producing one phenotype rather than the other. In the predator environment, genotypes 2 (G2) and 3 (G3) both produce the same 800 μm phenotype yet differ in fitness. As genotype 3 is plastic, this represents a cost of plasticity.

Figure 2

Developmental timepoint and impacts on evaluation of costs. For learning-like mechanisms of plasticity, performance varies over development as several phenotypes are expressed and the optimal phenotype is gradually adopted. Because performance varies over time, the developmental timepoint at which phenotype costs are measured can have a major impact on their interpretation. A specialist (dashed line) has a fixed performance that is higher in environmental one. The non-plastic generalist (solid line) has the same performance in both environments. The plastic genotype (dotted line) varies performance throughout developmental time. Thus, relative performance of the plastic and specialist genotypes may vary through developmental time or across environments.