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.

The evolution of sensitive periods in a model of incremental development

“…We find that selection favours phenotypic plasticity when there is high uncertainty early in development about the environmental state (e.g. the prior is close to 0.5) and cues are moderately or strongly informative [19]. If plasticity were costly, selection may favour non-plastic strategies (i.e.…”

“…individuals may vary in the extent to which the same experience shapes their development; [41]), (iii) between traits within a single individual (e.g. cognitive systems may adjust more easily than emotional systems to a radically changed environment; [11]), and (iv) within traits across development [19]. Our model generates such variation.…”

“…However, the costs of plasticity may vary across ontogeny (e.g. due to changing trade-offs between body parts) [19]. Introducing such a variable cost could favour more age-dependent plasticity.…”

The influence of weather conditions during gestation on life histories in a wild Arctic ungulate

“…There is now overwhelming evidence that 'early life' represents a sensitive window influencing the phenotype in various species [1,2]. Environmental conditions prevailing during this period, when the architecture of the body is being established [3], often show short-term effects, for instance by influencing juvenile survival [4].…”

Egg‐laying environment modulates offspring responses to predation risk in an amphibian

“…Indeed, variation in conditions during critical stages or periods during development has been proposed by previous works to have long‐lasting phenotypic consequences in many organisms’ life, even if the exposure is of short duration and/or of weak intensity (see examples in Taborsky, ; Massot & Aragón, ; Mueller et al ., ; Ferrari et al ., ). Moreover, the presence of such sensitive windows early on during development accords well with relevant theory (Fawcett & Frankenhuis, ).…”