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

      1 , 2 , 3 , 1
      Philosophical Transactions of the Royal Society B: Biological Sciences
      The Royal Society

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          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'.

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          Most cited references47

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          Developmental plasticity and human health.

          Many plants and animals are capable of developing in a variety of ways, forming characteristics that are well adapted to the environments in which they are likely to live. In adverse circumstances, for example, small size and slow metabolism can facilitate survival, whereas larger size and more rapid metabolism have advantages for reproductive success when resources are more abundant. Often these characteristics are induced in early life or are even set by cues to which their parents or grandparents were exposed. Individuals developmentally adapted to one environment may, however, be at risk when exposed to another when they are older. The biological evidence may be relevant to the understanding of human development and susceptibility to disease. As the nutritional state of many human mothers has improved around the world, the characteristics of their offspring--such as body size and metabolism--have also changed. Responsiveness to their mothers' condition before birth may generally prepare individuals so that they are best suited to the environment forecast by cues available in early life. Paradoxically, however, rapid improvements in nutrition and other environmental conditions may have damaging effects on the health of those people whose parents and grandparents lived in impoverished conditions. A fuller understanding of patterns of human plasticity in response to early nutrition and other environmental factors will have implications for the administration of public health.
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            A theory of human life history evolution: Diet, intelligence, and longevity

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              Hedging one's evolutionary bets, revisited.

              Evolutionary bet-hedging involves a trade-off between the mean and variance of fitness, such that phenotypes with reduced mean fitness may be at a selective advantage under certain conditions. The theory of bet-hedging was first formulated in the 1970s, and recent empirical studies suggest that the process may operate in a wide range of plant and animal species. Copyright © 1989. Published by Elsevier Ltd.
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                Author and article information

                Journal
                Philosophical Transactions of the Royal Society B: Biological Sciences
                Phil. Trans. R. Soc. B
                The Royal Society
                0962-8436
                1471-2970
                February 25 2019
                April 15 2019
                February 25 2019
                April 15 2019
                : 374
                : 1770
                : 20180109
                Affiliations
                [1 ]Liggins Institute, University of Auckland, New Zealand
                [2 ]Singapore Institute for Clinical Sciences, Singapore
                [3 ]Institute of Developmental Sciences, University of Southampton, Southampton SO17 1BJ, UK
                Article
                10.1098/rstb.2018.0109
                6460082
                30966891
                22ad464f-cc60-4286-8927-3fec5901c37c
                © 2019
                History

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