Fetal origins of developmental plasticity: are fetal cues reliable predictors of future nutritional environments?

Evidence that fetal nutrition triggers permanent adjustments in a wide range of systems and health outcomes is stimulating interest in the evolutionary significance of these responses. This review evaluates the postnatal adaptive significance of fetal developmental plasticity from the perspective of life history theory and evolutionary models of energy partitioning. Birthweight is positively related to multiple metabolically costly postnatal functions, suggesting that the fetus has the capacity to distribute the burden of energy insufficiency when faced with a nutritionally challenging environment. Lowering total requirements may reduce the risk of negative energy balance, which disproportionately impacts functions that are not essential for survival but that are crucial for reproductive success. The long-term benefit of these metabolic adjustments is contingent upon the fetus having access to a cue that is predictive of its future nutritional environment, a problem complicated in a long-lived species by short-term ecologic fluctuations like seasonality. Evidence is reviewed suggesting that the flow of nutrients reaching the fetus provides an integrated signal of nutrition as experienced by recent matrilineal ancestors, which effectively limits the responsiveness to short-term ecologic fluctuations during any given pregnancy. This capacity for fetal nutrition to minimize the growth response to transient ecologic fluctuations is defined here as intergenerational "phenotypic inertia," and is hypothesized to allow the fetus to cut through the "noise" of seasonal or other stochastic influences to read the "signal" of longer-term ecologic trends. As a mode of adaptation, phenotypic inertia may help the organism cope with ecologic trends too gradual to be tracked by conventional developmental plasticity, but too rapid to be tracked by natural selection. From an applied perspective, if a trait like fetal growth is designed to minimize the effects of short-term fluctuations by integrating information across generations, public health interventions may be most effective if focused not on the individual but on the matriline. (c) 2004 Wiley-Liss, Inc.