Trends in Ecology & Evolution
Predictive adaptive responses and human evolution
Introduction
Clinical and epidemiological research has identified numerous links between measures of early human development and the incidence of adult disease [1]. Most work has linked an impaired fetal environment, as reflected by small size at birth, to a greater risk of coronary heart disease and non-insulin dependent diabetes in middle-aged and elderly people 2, 3, 4. This relationship has been termed the ‘fetal (or developmental) origins of adult disease’ [2] because it suggests that events in early development irreversibly alter components of homeostasis in such a way that, when amplified or challenged by postnatal environmental factors, disease becomes manifest. Hales and Barker 1, 5 proposed this phenomenon to be the accidental effect of what they termed the ‘thrifty phenotype hypothesis’, an immediate fetal adaptation to altered nutrient supply that is mediated in part by insulin deficiency and/or resistance (insulin being a major fetal growth promoting hormone) for survival in a deficient intrauterine environment. These changes leave the growth-retarded fetus to cope with the consequences, which depend on whether the postnatal environment is nutritionally rich or poor. Experimental studies have readily replicated a relationship between early life experience and adult metabolic and cardiovascular function in a variety of mammal species [6]: the breadth of this demonstration suggests that some general biological process underpins it. Hales and Barker 1, 5 recognized that there might be postnatal advantage for a ‘thrifty’ phenotype in a nutritionally deprived environment. We 6, 7, 8 and others [9] have proposed that these observations can be better interpreted as part of a broader set of developmental and evolutionary strategies that we have termed ‘predictive adaptive responses’ (PARs) 6, 8. Placing these strategies in this perspective has important implications for understanding changing patterns of human disease.
Section snippets
Predictive adaptive responses
We define PARs as a form of developmental plasticity that evolved as adaptive responses to environmental cues acting early in the life cycle, but where the advantage of the induced phenotype is primarily manifest in a later phase of the life cycle. The cue affects the processes of developmental plasticity and thus induces changes in the developmental trajectory of form and function such that the organism presets its physiology in expectation of that physiology matching its future environment.
Developmental responses
When considering effects of the environment on development, it is important to distinguish between responses that might be adaptive later in life from those that (i) merely disrupt development in a pathological manner (e.g. those causing fetal malformation) leaving the organism to ‘cope’ with the consequences [28]; and (ii) involve immediate adaptation for fetal survival (e.g. fetal growth retardation) having an incidental advantage later. Some responses to environmental stress could be
A general model of PARs
The presence of many similar PARs in diverse groups of organisms suggests that the capacity to induce PARs is adaptive [8]. This assumption implies that there has been an advantage in retaining and refining PARs because fetal predictive responses have generally been appropriate for the postnatal environment, and this choice has conferred a selective advantage on the bearers. In our view, it is the ability to mount a PAR itself that constitutes an adaptation, not only the phenotypes that it
Maternal constraint, normal variation in fetal growth and PARs
Variation in postnatal growth has a major genetic component, whereas fetal growth is more environmentally sensitive. This difference is revealed, for example, in the far greater correlation between siblings in adult height than in birth size [41]. The environment of the fetus is created by its mother and, once developed, by the placenta. Maternal factors must dominate in determining fetal growth because the mammalian fetus will not survive if it outgrows the pelvic canal of its mother. Thus, it
Conclusion and future directions
PARs are a form of phenotypic plasticity with delayed selective benefits seen in many species. We argue that they have been retained in humans because they conferred survival advantage in the poorer nutritional and high-energy expenditure environment of our ancestral hominids. PARs are induced by environmental cues in development, utilizing the normal processes of maternal constraint as part of the mechanism of providing environmental cues to the fetus. In our evolutionary past, it was
Acknowledgements
We thank Patrick Bateson for many discussions. Comments from the referees also led to a significant improvement in the article. M.A.H. is supported by the British Heart Foundation.
References (60)
Fetal programming of coronary heart disease
Trends Endocrinol. Metab.
(2002)- et al.
The developmental origins of the metabolic syndrome
Trends Endocrinol. Metab.
(2004) - et al.
The physiology of locust phase polymorphism: an update
J. Insect Physiol.
(1998) - et al.
Compensation for a bad start: grow now or pay later?
Trends Ecol. Evol.
(2001) - et al.
Early origins of cardiovascular disease: is there a unifying hypothesis?
Lancet
(2004) Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat
Life Sci.
(1999)Maternal dietary protein restriction in pregnant rats induces epigenetic modification of hepatic gene expression in the offspring which is preventable by maternal dietary folic acid supplementation
J. Nutr.
(2005)- et al.
Genetic regulatory mechanisms in the synthesis of proteins
J. Mol. Biol.
(1961) - et al.
The adaptive significance of maternal effects
Trends Ecol. Evol.
(1998) Early development and fitness in birds and mammals
Trends Ecol. Evol.
(1999)