Adaptive explanations for sensitive windows in development

Abstract

Development in many organisms appears to show evidence of sensitive windows-periods or stages in ontogeny in which individual experience has a particularly strong influence on the phenotype (compared to other periods or stages). Despite great interest in sensitive windows from both fundamental and applied perspectives, the functional (adaptive) reasons why they have evolved are unclear. Here we outline a conceptual framework for understanding when natural selection should favour changes in plasticity across development. Our approach builds on previous theory on the evolution of phenotypic plasticity, which relates individual and population differences in plasticity to two factors: the degree of uncertainty about the environmental conditions and the extent to which experiences during development ('cues') provide information about those conditions. We argue that systematic variation in these two factors often occurs within the lifetime of a single individual, which will select for developmental changes in plasticity. Of central importance is how informational properties of the environment interact with the life history of the organism. Phenotypes may be more or less sensitive to environmental cues at different points in development because of systematic changes in (i) the frequency of cues, (ii) the informativeness of cues, (iii) the fitness benefits of information and/or (iv) the constraints on plasticity. In relatively stable environments, a sensible null expectation is that plasticity will gradually decline with age as the developing individual gathers information. We review recent models on the evolution of developmental changes in plasticity and explain how they fit into our conceptual framework. Our aim is to encourage an adaptive perspective on sensitive windows in development.

Keywords: Adaptive developmental plasticity; Autocorrelation; Bayesian updating; Behavioural consistency; Critical period; Cue reliability; Environmental predictability; Social behaviour; Value of information.

Figure 1

Selection for fixed versus plastic phenotypes. This schematic representation (inspired by [28,30]) shows how evolved plasticity should depend on uncertainty about environmental conditions and the informativeness of cues received during development. Plasticity (dark shading) is favoured when high uncertainty about environmental conditions is combined with cues that are highly informative about those conditions; otherwise, a fixed phenotype is favoured. Note that both of these factors (uncertainty about conditions and informativeness of cues) may change during ontogeny. For example, uncertainty will tend to decrease over development (as indicated by the white block arrows), particularly if the cues received are highly informative; this will weaken the benefits of plasticity later in life (all else being equal).

Figure 2

Developmental changes in information state when conditions are stable. The upper panel shows the optimal estimate (p_t) of the environmental state in response to a steady stream of information (from cues of fixed reliability), calculated using Bayesian updating (Appendix A, additional file 1). The lower panel shows the extent to which the estimate changes (Δp_t) when a new cue is observed. The three different lines depict the estimates for individuals in three cases, depending on whether the initial estimate is a uniform prior (i.e. both states are equally likely), is in agreement with subsequent cues (‘congruent’) or is contradicted by subsequent cues (‘incongruent’ ). Note that sensitivity to environmental cues declines with time, unless the observed cues contradict the initial estimate. See text for more details.

Figure 3

Developmental changes in information state when conditions change. As for Fig. 2, except that uncertainty increases mid-way through development because individuals encounter a new social situation. For clarity, only the trajectory with the uniform prior is shown. See text for more details.