Quantitative assessment of the importance of phenotypic plasticity in adaptation to climate change in wild bird populations

Abstract

Predictions about the fate of species or populations under climate change scenarios typically neglect adaptive evolution and phenotypic plasticity, the two major mechanisms by which organisms can adapt to changing local conditions. As a consequence, we have little understanding of the scope for organisms to track changing environments by in situ adaptation. Here, we use a detailed individual-specific long-term population study of great tits (Parus major) breeding in Wytham Woods, Oxford, UK to parameterise a mechanistic model and thus directly estimate the rate of environmental change to which in situ adaptation is possible. Using the effect of changes in early spring temperature on temporal synchrony between birds and a critical food resource, we focus in particular on the contribution of phenotypic plasticity to population persistence. Despite using conservative estimates for evolutionary and reproductive potential, our results suggest little risk of population extinction under projected local temperature change; however, this conclusion relies heavily on the extent to which phenotypic plasticity tracks the changing environment. Extrapolating the model to a broad range of life histories in birds suggests that the importance of phenotypic plasticity for adjustment to projected rates of temperature change increases with slower life histories, owing to lower evolutionary potential. Understanding the determinants and constraints on phenotypic plasticity in natural populations is thus crucial for characterising the risks that rapidly changing environments pose for the persistence of such populations.

Figure 1. Annual mean great tit laying date and annual caterpillar half-fall date in Wytham Woods plotted against spring temperature.

The trend line for laying date represents the average within-individual response to spring temperature (see Results). The trend line for half-fall date represents the average response to spring temperature.

Figure 2. Frequency distribution of model predicted critical rate of temperature change that allows population persistence (η _c) , (a) based on 100,000 simulations randomly sampling from error distributions of parameters σ²h², γ, T, B and b, estimated for great tits in Wytham Woods (see Table 1).

The dashed vertical line represents the predicted rate of local temperature change, under the high emissions scenario . Note that the distribution is highly skewed, with the modal outcome being biased to lower values of η _c and a long tail of high values of η _c (for visual purposes the x-axis was cut off at η _c = 1.0). This is because the difference between the reaction norm of great tit laying date in response to spring temperature (b) and the optimal reaction norm (B) is modelled in absolute terms while in the simulations b often exceeds B, causing the average outcome of |B−b| to be higher than the outcome for the point estimate. (b) Frequency distribution of η _c, based on 100,000 simulations randomly sampling from error distributions of parameters σ²h², γ, and T, assuming there is no phenotypic plasticity (for this population, |B−b| = 5.30). The dashed vertical line represents the predicted rate of local temperature change, under the high emissions scenario . Note that the scale on the x-axis differs between the two figures.

Figure 3. Probability of population extinction (η _c<0.030), based on 100,000 simulations incorporating the error distribution of parameter estimates, plotted for (a) r_max and T, assuming the observed phenotypic plasticity (|B−b| = 0.32), (b) r_max and T, assuming there is no phenotypic plasticity (|B−b| = 5.30), (c) γ and σ²h² (for laying date) assuming the observed phenotypic plasticity (|B−b| = 0.32), (d) γ and σ²h² (for laying date) assuming no phenotypic plasticity (|B−b| = 5.30).

Open circles and solid trend line in (b) represent estimates for r_max and T of 13 bird species, and their derived interrelationship (r_max = 0.92T ^−0.92), illustrating a general life-history pattern in birds . The dashed lines in (a, c, and d) represent the estimated values for the parameter on the axis, for Wytham Woods' great tits (see Table 1).

Figure 4. Probability of population extinction (η _c<0.030) plotted for generation time (T) and the mismatch between the observed and optimal phenotypic response to temperature (|B−b|), assuming r_max = 0.92T ^−0.92 and incorporating the error distribution of γ and σ²h² as estimated for Wytham Woods' great tits.