The biology of developmental plasticity and the Predictive Adaptive Response hypothesis

Abstract

Many forms of developmental plasticity have been observed and these are usually beneficial to the organism. The Predictive Adaptive Response (PAR) hypothesis refers to a form of developmental plasticity in which cues received in early life influence the development of a phenotype that is normally adapted to the environmental conditions of later life. When the predicted and actual environments differ, the mismatch between the individual's phenotype and the conditions in which it finds itself can have adverse consequences for Darwinian fitness and, later, for health. Numerous examples exist of the long-term effects of cues indicating a threatening environment affecting the subsequent phenotype of the individual organism. Other examples consist of the long-term effects of variations in environment within a normal range, particularly in the individual's nutritional environment. In mammals the cues to developing offspring are often provided by the mother's plane of nutrition, her body composition or stress levels. This hypothetical effect in humans is thought to be important by some scientists and controversial by others. In resolving the conflict, distinctions should be drawn between PARs induced by normative variations in the developmental environment and the ill effects on development of extremes in environment such as a very poor or very rich nutritional environment. Tests to distinguish between different developmental processes impacting on adult characteristics are proposed. Many of the mechanisms underlying developmental plasticity involve molecular epigenetic processes, and their elucidation in the context of PARs and more widely has implications for the revision of classical evolutionary theory.

Figure 1. Relationship between nutritional plane and Darwinian fitness as an adult

The diagram shows the proposed relationship between the environment (e.g. nutritional plane) to which the developing organism is exposed during the phase of developmental plasticity and the consequences for its Darwinian fitness in adult life. The relationship is determined by different mechanisms according to the degree of shift in the environmental state from the optimal, as suggested by the shaded columns. (From Gluckman et al. .)

Figure 2. A given genotype may give rise to different phenotypes depending on the state of the environment early in development

Cues from the environment may be used as predictors, determining which of a set of alternative developmental pathways is elicited. If the environment does not change, then the organism's phenotype will be well adapted to that environment, providing a close match, as is represented in the diagram by the pattern and shape of the phenotype and the pattern and shape of the environment. However, if the environment does change between the elicitation of the particular pattern and development, then the phenotype may be mismatched to the conditions of adult life. (From Bateson .)

Figure 3. Different factors that may affect the survival and reproductive success of an individual

On the lowest plane of nutrition the individual may suffer developmental disruption or be forced to sacrifice future reproductive success in order to survive. On a plane of nutritional excess individuals are likely to suffer health problems. On intermediate levels of nutrition the degree of the match between the predicted and the actual environment is crucial, according to the PAR hypothesis.