Costs and limits of phenotypic plasticity

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Abstract

The costs and limits of phenotypic plasticity are thought to have important ecological and evolutionary consequences, yet they are not as well understood as the benefits of plasticity. At least nine ideas exist regarding how plasticity may be costly or limited, but these have rarely been discussed together. The most commonly discussed cost is that of maintaining the sensory and regulatory machinery needed for plasticity, which may require energy and material expenses. A frequently considered limit to the benefit of plasticity is that the environmental cues guiding plastic development can be unreliable. Such costs and limits have recently been included in theoretical models and, perhaps more importantly, relevant empirical studies now have emerged. Despite the current interest in costs and limits of plasticity, several lines of reasoning suggest that they might be difficult to demonstrate.

Section snippets

Costs versus limits of plasticity

The benefit of plasticity is the ability to produce a better phenotype-environment match across more environments than would be possible by producing a single phenotype in all environments[17]. If constraints did not exist, organisms should exhibit `perfect' or `infinite' plasticity, expressing the best trait value in every environment with no cost for having that ability. Generally, plastic organisms fail this ideal because of an inability to consistently produce the optimum (i.e. a

Maintenance costs

Maintenance costs could be incurred by plastic organisms if facultative development requires the maintenance of sensory and regulatory machinery that fixed development does not require5, 11, 13, 18. For example, the ethylene growth response in plants requires the response of an ethylene receptor protein on the cell membranes of plants[19]. If development were insensitive to ethylene, the energetic and material cost of producing the receptor protein (i.e. the sensory machinery) could be saved.

Production costs

Information reliability limits

As noted earlier, producing a plastic response may require information about the environment. In addition to the cost of information acquisition, however, there can be problems associated with poor reliability of cues used to assess the environment11, 13, 14, 17, 23, 24, 33. Plastic organisms with unreliable information express poor phenotype-environment matching.

Lag-time limits

Temporary problems with poor phenotype-environment matching can also be generated by a lag-time between sensing and responding to

What are the odds of detecting costs?

Here we question three expectations that underlie the search for costs of plasticity: (1) the expectation that plasticity is necessarily costly, (2) the expectation that costly but nonadaptive plasticity should persist in nature, and (3) the expectation that plasticity will remain costly over evolutionary time.

First, whether we expect plasticity or constancy to be more costly depends on whether the focal trait exhibits plasticity as an `active' or `passive' (sensu Ref. [10]) response to

Measuring plasticity costs

Although plasticity is easily documented without quantifying genetic relationships among organisms (e.g. Refs [38]and [39]), the parameters needed to detect costs of plasticity require controlled quantitative genetic experimental designs5, 12. Generally, related groups of individuals (full or half sibships, clones, etc.) are raised in two or more environments to estimate components of phenotypic variation due to genetic affiliation, environment and genotype-environment interactions. Each

Future directions

Models have already demonstrated several ecological and evolutionary consequences of various constraints on plasticity. Modeling these constraints may continue to be useful, but without good empirical data it is difficult to know which constraints are most likely or what magnitude each assumes. For example, as costs are documented empirically, we will have data to use in existing models, so that predictions about particular empirical systems can be made. The first researchers to document costs

Acknowledgements

We thank Sam Scheiner, Massimo Pigliucci, Chris Grill and Carl Schlichting for valuable input. Preparation of this paper was supported by the US National Science Foundation (grant DEB-9618702 to T.J.D. and A.S.).

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