Abstract

Abstract Two extant evolutionary models, biological sensitivity to context theory (BSCT) and differential susceptibility theory (DST), converge on the hypothesis that some individuals are more susceptible than others to both negative (risk-promoting) and positive (development-enhancing) environmental conditions. These models contrast with the currently dominant perspective on personal vulnerability and environmental risk: diathesis stress/dual risk. We review challenges to this perspective based on emerging theory and data from the evolutionary, developmental, and health sciences. These challenges signify the need for a paradigm shift in conceptualizing Person  Environment interactions in development. In this context we advance an evolutionary-neurodevelopmental theory, based on DST and BSCT, of the role of neurobiological susceptibility to the environment in regulating environmental effects on adaptation, development, and health. We then outline current thinking about neurogenomic and endophenotypic mechanisms that may underpin neurobiological susceptibility, summarize extant empirical research on differential susceptibility, and evaluate the evolutionary bases and implications of BSCT and DST. Finally, we discuss applied issues including methodological and statistical considerations in conducting differential susceptibility research; issues of ecological, cultural, and racial-ethnic variation in neurobiological susceptibility; and implications of differential susceptibility for designing social programs. We conclude that the differential susceptibility paradigm has far-reaching implications for understanding whether and how much child and adult development responds, for better and for worse, to the gamut of species-typical environmental conditions. Decades of research demonstrate that exposure to environmental adversity places children and adults at elevated risk for developing cognitive, social, emotional, and health problems 1. Individuals characterized by heightened environmental susceptibility display enhanced sensitivity to both negative and positive environments, that is, to both risk-promoting and development-enhancing environmental conditions. 2. This enhanced sensitivity increases developmental receptivity to the environment. That is, more susceptible individuals are more likely to experience sustained developmental change, not just transient fluctuations in functioning, in response to environmental exposures 3. Susceptibility to the environment is instantiated in the biology of the nervous system; it is neurobiological susceptibility. Genetic susceptibility factors operate through 7 neurobiological processes and behavioral indicators of susceptibility are grounded in neurobiology. 4. Developmental experience plays a role, along with heritable polygenic variation, in determining individual differences in neurobiological susceptibility. 5. Individuals of all ages (children and adults) vary in neurobiological susceptibility to environmental influences and, within individuals, susceptibility may vary across the life span. 6. Individual differences in neurobiological susceptibility are adaptive in the evolutionary sense and have been conserved by fluctuating selective pressures that generate different fitness payoffs across different social, physical, and historical contexts (or at least did so during the course of human evolution). 7. Variation in neurobiological susceptibility to the environment, therefore, constitutes a central mechanism in the regulation of alternative patterns of human development; specifically, differential susceptibility moderates the effects of environmental exposures on developmental and life outcomes. Ultimately, this means that the development of some individuals, more than others, will be influenced by their experiences and environments (even if these were exactly the same). We begin this paper by outlining the defining features of the currently dominant perspective on environmental risk and human frailty: diathesis-stress/dual risk. We then review challenges to this perspective based on emerging theory and data from the evolutionary, developmental, and health sciences. These challenges highlight the need for a paradigm shift in conceptualizing Person  Environment interactions in development. In this context we frame an evolutionaryneurodevelopmental theory of how individual differences in neurobiological susceptibility to the environment may account for the impressive variation in the potency of environmental effects on adaptation, development, and health. The Dominant Paradigm: Diathesis-Stress/Dual Risk Students of human development widely appreciate that individuals vary in whether and how much they are negatively affected by environmental stressors, ranging from exposures to poverty to hostile or insensitive parenting to low quality child care, to name just a few well-studied phenomena. Perhaps the most striking evidence that personal characteristics condition or moderate such environmental effects is found in developmental research on Temperament  Parenting interactions The "dual-risk" designation derives from the synergistic effect of a risk (or diathesis) inherent in the individual interacting with one operative in the environment. Where some people are regarded as especially susceptible to adversity because of their personal vulnerabilities, other people lacking such vulnerabilities who do not succumb to the adversity in question are considered to be resilient Beyond Diathesis-Stress/Dual Risk: Evolutionary Models of Adaptive Development An evolutionary perspective challenges the prevailing developmental psychopathological analysis of dysfunctional or maladaptive outcomes within settings of adversity. In particular, it contends that both stressful and supportive environments have been part of human experience throughout our evolutionary history, and that developmental systems shaped by natural selection respond adaptively to both kinds of contexts. Thus, when people encounter stressful environments, this does not so much disturb their development as direct or regulate it toward strategies that are adaptive under stressful conditions, even if those strategies are currently harmful in terms of the long-term welfare of the individual or society as a whole (see B. J. Ellis et al. 8 Consider the extensive experimental work conducted by Michael Meaney and colleagues showing that putatively low quality maternal care in the rat (i.e., low levels of maternal licking and grooming) alters pups' stress physiology and brain morphology. Although such changes seem disadvantageous (i.e., higher corticosterone levels, shorter dendritic branch lengths, and lower spine density in hippocampal neurons), they actually enhance learning and memory processes under stressful conditions It is important to note that optimal adaptation (in the evolutionary sense) to challenging environments is not without real consequences and costs. Harsh environments often harm or kill children, and the fact that children developmentally adapt to such rearing conditions (reviewed in Ellis,