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

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

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’.

Development, Developmental plasticity, Evolution, Mismatch, Predictive adaptive response, Trade-offs
0962-8436
1-8
Gluckman, Peter D.
20557908-bee4-4c9f-bcca-950e8de3d704
Hanson, Mark A.
1952fad1-abc7-4284-a0bc-a7eb31f70a3f
Low, Felicia M.
0f67b4e9-9879-4227-b9e3-10af72a26dc0
Gluckman, Peter D.
20557908-bee4-4c9f-bcca-950e8de3d704
Hanson, Mark A.
1952fad1-abc7-4284-a0bc-a7eb31f70a3f
Low, Felicia M.
0f67b4e9-9879-4227-b9e3-10af72a26dc0

Gluckman, Peter D., Hanson, Mark A. and Low, Felicia M. (2019) Evolutionary and developmental mismatches are consequences of adaptive developmental plasticity in humans and have implications for later disease risk. Philosophical Transactions of the Royal Society B: Biological Sciences, 374 (1770), 1-8, [20180109]. (doi:10.1098/rstb.2018.0109).

Record type: Review

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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More information

Accepted/In Press date: 31 October 2018
e-pub ahead of print date: 25 February 2019
Published date: April 2019
Keywords: Development, Developmental plasticity, Evolution, Mismatch, Predictive adaptive response, Trade-offs

Identifiers

Local EPrints ID: 431414
URI: http://eprints.soton.ac.uk/id/eprint/431414
ISSN: 0962-8436
PURE UUID: 7133ca97-8a51-4ed8-bd61-730a748076cc
ORCID for Mark A. Hanson: ORCID iD orcid.org/0000-0002-6907-613X

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Date deposited: 31 May 2019 16:30
Last modified: 06 Jun 2024 01:39

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Contributors

Author: Peter D. Gluckman
Author: Mark A. Hanson ORCID iD
Author: Felicia M. Low

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