Phenotypic plasticity is a term familiar to evolutionary biologists. It refers to the ability of an organism to respond to a changing environment by changing its physical properties – its phenotype. For example, metabolic rate changes with temperature and resource availability.

We usually assume that such changes are adaptive, that is, changes are in the same direction as selection and so will increase the fitness (reproductive output) of the organism in that environment. But, importantly, we don’t usually test for the adaptive significance of phenotypic plasticity because we don’t typically estimate selection in different environments when we assess plasticity.

Lukas Schuster and his supervisors, Craig White and Dustin Marshall, used the model species Bugula neritina to investigate whether changes in metabolic rates in response to different field environments are an example of adaptive phenotypic plasticity. To their surprise they found that, while Bugula exhibited plasticity in metabolic rate, it was not adaptive.

Bugula is a small filter feeding colonial bryozoan that is often found on the undersides of piers. It is also found on vertical surfaces such as pier pilings, although the increased UV radiation and sedimentation experienced on vertical surfaces combine to make this a more stressful living environment.

Lukas collected mature colonies of Bugula from the field and then spawned them in the laboratory and settled the larvae onto small acetate sheets. This allowed Lukas to deploy the Bugula on vertically or horizontally suspended panels (corresponding to harsh and benign environments respectively) and to return colonies to the laboratory to measure metabolic rates. They did two experimental runs to test the consistency of the results.

As a first step, Lukas and his supervisors had to determine how selection on metabolic rate varies across harsh and benign environments. In other words, they needed to establish the relationship between metabolic rate and reproductive output (fitness) in each environment.

They deployed newly settled Bugula to a common, benign environment for three weeks before returning these colonies to the laboratory to measure metabolic rates. Half of the colonies were then deployed into the harsh environment and half was kept in the benign environment. Growth, survival and lifetime reproductive output were then tracked for each colony; this allowed the team to determine whether there was any fitness advantage associated with particular metabolic rates in each environment.

Surprisingly, they found no differences in selection on metabolic rates in the two environments. Instead, in one experimental run, they found evidence that smaller individuals with lower metabolic rates and larger individuals with higher metabolic rates went on to produce more offspring in both environments. This suggests that metabolic rate is unlikely to evolve independently of other traits.

To measure plasticity Lukas returned all colonies to the laboratory to measure metabolic rates for a second time. Colonies from the harsh environment had overall lower metabolic rates compared to colonies from the benign environment.

Given the strong and consistent metabolic response to the different environments that the team observed, it would have been tempting to infer that such a response increases fitness. While this seems intuitive, it is not consistent with what they know about selection on metabolic rate in the different environments. There was no difference in the relationship between metabolic rates and reproductive outputs in the two environments and so, although the changes they saw in metabolic rate with environment show that metabolic rate is plastic, their results show that such plasticity is not always adaptive.

Lukas and his supervisors emphasise the importance of assessing selection on a trait in the different environments before assuming that ‘plastic’ responses to different environments are necessarily adaptive. Instead, metabolic plasticity may merely represent a passive response due to correlations with other traits or there may be limits to physiological plasticity due to biochemical constraints. Nonetheless, further studies are needed in order to understand the drivers and consequences of metabolic plasticity in the field.

This research was published in the journal Oikos.