Evolutionary and developmental mismatches are consequences of adaptive developmental plasticity in humans and have implications for later disease risk

Abstract

A discrepancy between the phenotype of an individual and that which would confer optimal responses in terms of fitness in an environment is termed ‘mismatch’. Phenotype results from developmental plasticity, conditioned partly by evolutionary history of the species and partly by aspects of the developmental environment. We discuss two categories of such mismatch with reference primarily to nutrition and in the context of evolutionary medicine. The categories operate over very different timescales. A developmental mismatch occurs when the phenotype induced during development encounters a different environment post-development. This may be the result of wider environmental changes, such as nutritional transition between generations, or because maternal malnutrition or placental dysfunction give inaccurate information about the organism's likely future environment. An evolutionary mismatch occurs when there is an evolutionarily novel environment. Developmental plasticity may involve immediate adaptive responses (IARs) to preserve survival if an environmental challenge is severe, and/or predictive adaptive responses (PARs) if the challenge does not threaten survival, but there is a fitness advantage in developing a phenotype that will be better adapted later. PARs can have long-term adverse health consequences if there is a developmental mismatch. For contemporary humans, maternal constraint of fetal growth makes PARs likely even if there is no obvious IAR, and this, coupled with the pervasive nutritionally dense modern environment, can explain the widespread observations of developmental mismatch, particularly in populations undergoing nutritional transition. Both developmental and evolutionary mismatch have important public health consequences and implications for where policy interventions may be most effective. This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine'.

Developmental responses to early‐life adversity: Evolutionary and mechanistic perspectives

“…Under this model, the high prevalence of noncommunicable disease in low birth weight individuals is not viewed as a life history tradeoff, but rather a consequence of modern human diets creating a mismatch between the prenatal and adult environments. Importantly, Gluckman and Hanson recently pointed out that, contrary to what has been assumed in the literature, the PAR model does not assume that individuals raised in adverse environments experience no constraints—only that those constraints are at least alleviated if not erased by adaptive developmental calibrations …”

“…Despite these findings, some researchers have suggested a more cautious interpretation of the data . A major weakness of previous studies is that fitness outcomes associated with matched and unmatched conditions were assumed to be fairly homogenous across individuals (i.e., individuals all develop the same developmental responses to environmental gradients).…”

“…Such data are not only rare, but particularly difficult to interpret in modern humans, for which rapid improvements in medicine and birth control may cloud the interpretation of existing data. Furthermore, in the few cases where empirical data on nonhuman species have been brought forth, debate remains over whether these studies have accurately tested the fundamental hypotheses of each model …”

“…Furthermore, in the few cases where empirical data on nonhuman species have been brought forth, debate remains over whether these studies have accurately tested the fundamental hypotheses of each model. 31,33 A common approach in recent years is to use a 2-by-2 factorial framework to tease apart whether early-life adversity primarily leads to fitness constraints (i.e., developmental constraints) or adaptive advantages when later-life environments are matched (i.e., PAR). 17,21 While the developmental constraints model predicts that early-life adjustments lead to reduced fitness, which might be exacerbated but When fitness data have been used to test the predictions of these models, they have mostly been interpreted as supporting developmental constraints over PAR (see recent reviews 17,32 ), particularly in longlived mammals.…”

“…Despite these findings, some researchers have suggested a more cautious interpretation of the data. 31,33 A major weakness of previous studies is that fitness outcomes associated with matched and unmatched conditions were assumed to be fairly homogenous across individuals (i.e., individuals all develop the same developmental responses to environmental gradients). If this assumption is violated, however, the failure to identify later-life fitness benefits may be a methodological artifact of lumping individuals that initiated adaptive developmental responses with those that did not.…”