Re-evaluating the costs and limits of adaptive phenotypic plasticity

Abstract

When the optimal phenotype differs among environments, adaptive phenotypic plasticity can evolve unless constraints impede such evolution. Costs and limits of plasticity have been proposed as important constraints on the evolution of plasticity, yet confusion exists over their distinction. We attempt to clarify these concepts by reviewing their categorization and measurement, highlighting how costs and limits are defined in different currencies (and may describe the same phenomenon). Conclusions from studies that measure the costs of plasticity have been equivocal, but we caution that these conclusions may be premature owing to a potentially common correlation between environment-specific trait values and the magnitude of trait plasticities (i.e. multi-collinearity) that results in imprecise and/or biased estimates of the costs. Meanwhile, our understanding of the limits of plasticity, and how they may be underlain by the costs of plasticity, is still in its infancy. Based on our re-evaluation of these constraints, we discuss areas for future research.

Figure 1.

Hypothetical relationships for genotypes that differ in phenotypic value and magnitude of plasticity. (a) A population of genotypes that shows independence between phenotypic values and magnitudes of plasticity. (b,c) Populations of genotypes that show independence between phenotypic values and magnitudes of plasticity in one environment but not in the other. (d) A population of genotypes showing no independence between phenotypic values and magnitudes of plasticity in either environment.

Figure 2.

The relationship between trait values and trait plasticities (i.e. the difference in trait values across environments) for several traits in three species; all data points are family means. In all cases, the most plastic families exhibit the most extreme trait values. (a–c) Traits of larval wood frogs (Rana sylvatica) reared with (closed symbols) or without (open symbols) predators (Relyea 2002; plotted trait values are size-independent residuals from the linear regression of log-transformed trait values against log-transformed mass). (d) A morphological defence of freshwater snails (Physa acuta) reared with (closed) or without (open) predator cues and (e) a life-history trait from the same species reared with (closed) and without (open) mates (J. R. Auld 2009, unpublished manuscript). (f) A chemical-defence trait of wild radishes (Raphanus raphanistrum) when reared with (closed) and without (open) herbivore damage (Agrawal et al. 2002). Correlations between trait values and trait plasticities are provided as r² values within each environment.