The Adaptive Calibration Model of stress responsivity

Abstract

This paper presents the Adaptive Calibration Model (ACM), an evolutionary–developmental theory of individual differences in the functioning of the stress response system. The stress response system has three main biological functions: (1) to coordinate the organism's allostatic response to physical and psychosocial challenges; (2) to encode and filter information about the organism's social and physical environment, mediating the organism's openness to environmental inputs; and (3) to regulate the organism's physiology and behavior in a broad range of fitness-relevant areas including defensive behaviors, competitive risk-taking, learning, attachment, affiliation and reproductive functioning. The information encoded by the system during development feeds back on the long-term calibration of the system itself, resulting in adaptive patterns of responsivity and individual differences in behavior. Drawing on evolutionary life history theory, we build a model of the development of stress responsivity across life stages, describe four prototypical responsivity patterns, and discuss the emergence and meaning of sex differences. The ACM extends the theory of biological sensitivity to context (BSC) and provides an integrative framework for future research in the field.

Introduction

The stress response system (SRS) is an ancient biological mechanism, fine-tuned by natural selection and crucially involved in a wide range of adaptive functions in humans as well as other animals. The basic structure of the SRS is highly conserved across species (Nesse et al., 2007); however, the SRS exhibits a striking amount of individual variation in its working parameters (e.g., baseline activation, hormone levels) and in its responsivity to external events (e.g., the magnitude of cortisol response, or the balance between sympathetic and parasympathetic activation). In turn, individual differences in stress responsivity consistently relate to differences in psychological functioning, social relations, and in the risk for mental and physical disorders. The SRS is highly plastic, especially in response to early experience (e.g., Boyce and Ellis, 2005, Gunnar et al., 2009a, Levine, 2005, Parker et al., 2006); at the same time, widespread allelic variation exists in many genes that can affect SRS functioning (e.g., Alexander et al., 2009, Alexander et al., 2011, Ouellet-Morin et al., 2008, Propper et al., 2008, Wüst et al., 2004). Understanding individual differences in stress responsivity – their causes, effects, and developmental processes leading to different patterns of responsivity – has become a major research focus in neuroscience, psychology, and medicine (e.g., Cameron et al., 2005, Ellis et al., 2006, Gunnar et al., 2009a, Korte et al., 2005). To date, however, a unifying theoretical framework for the study of individual differences in SRS functioning is still lacking.

In this paper we advance an evolutionary model of the development of stress responsivity in humans: the Adaptive Calibration Model (ACM). Our aim is to develop a biologically rigorous framework to understand the meaning of individual differences in responsivity and describe the developmental trajectories leading to such differences. The ACM is an extension of the theory of biological sensitivity to context (BSC; Boyce and Ellis, 2005, Ellis et al., 2005, Ellis and Boyce, 2008); to our knowledge, the ACM is the first theory of stress development to take full advantage of the tools of modern evolutionary and developmental biology. In particular, our model draws extensively on life history theory (Ellis et al., 2009, Roff, 2002), sexual selection and parental investment theory (Trivers, 1972, Kokko and Jennions, 2008), and the theory of developmental plasticity (West-Eberhard, 2003).

The ACM postulates that individual differences in stress responsivity are largely (though not exclusively) the result of conditional adaptation – the evolved ability of an organism to modify its developmental trajectory (and the resulting phenotype) to match the local conditions of the social and physical environment. Individual variation in responsivity is primarily seen as the result of adaptive mechanisms, rather than the outcome of pathological or dysfunctional processes. In the framework developed here, the SRS has three main biological functions: (1) to coordinate the organism's allostatic response to physical and psychosocial challenges; (2) to encode and filter information about the organism's social and physical environment, mediating the organism's openness to environmental inputs; and (3) to regulate the organism's physiology and behavior in a broad range of fitness-relevant areas including growth, competitive risk-taking, learning, attachment, affiliation, and reproductive functioning. All these traits and behaviors can be seen as components of the organism's life history (LH) strategy, a biological construct describing the developmental schedule of an organism and its allocation of time and energy to different fitness-promoting activities, such as mating and parenting (Fig. 1).

The central concept of the ACM is that information encoded by the SRS in the course of development feeds back on the long-term calibration of the system itself, resulting in adaptive patterns of responsivity and individual differences in life history-related behavior (the curved arrow in Fig. 1). In other words, the SRS acts as an integrative mechanism, mediating the development of alternative LH strategies that are adaptive in different environmental conditions (or at least have been adaptive during the course of human evolution). In this paper we describe the evolutionary logic of adaptive calibration and employ that logic to model a number of developmental trajectories – from birth to adulthood – that lead to stable patterns of individual differences in responsivity to environmental threats and opportunities.

Developmental psychologists frequently consider the effects of life experience on development but rarely consider how these effects have been structured by natural selection. Despite this oversight, the burgeoning field of evolutionary–developmental biology has exciting and profound implications for the study of human development (see especially West-Eberhard, 2003). Over the last two decades, theory and research in the field has come to acknowledge that, in most species, single “best” strategies for survival and reproduction are unlikely to evolve. This is because the “best” strategy varies as a function of the physical, economic, and socioemotional parameters of one's environment (Crawford and Anderson, 1989), and thus a strategy that promotes success in some environmental contexts may lead to failure in others (Belsky et al., 1991, Ellis and Boyce, 2008, Meaney, 2010). This adaptationist perspective challenges the prevailing notion (e.g., Beauchaine et al., 2007, Cicchetti and Rogosch, 2001, El-Sheikh et al., 2009, Evans and Kim, 2007) that childhood exposures to stress and adversity routinely derail normal development (i.e., induce dysregulated biological and behavioral functioning). Rather, both stressful and supportive environments have been part of the human experience throughout our evolutionary history, and thus our developmental systems have been shaped by natural selection to respond adaptively to a range of different contexts. 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; conversely, when people encounter well-resourced and supportive environments, it directs or regulates development toward strategies that are adaptive in that context (Ellis et al., 2011a, Ellis et al., 2011b, Flinn, 2006).

Consider the extensive experimental work conducted by Michael Meaney and colleagues, showing that relatively 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 may 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 (Bagot et al., 2009, Champagne et al., 2008). Moreover, such physiological and morphological changes mediate the effects of maternal behavior on central features of defensive and reproductive strategies: behavior under threat, open-field exploration, pubertal development, sexual behavior, and parenting (Cameron et al., 2005, Cameron et al., 2008a, Cameron et al., 2008b). In the rodent model presented by Meaney and colleagues, then, variations in stress physiology and brain morphology apparently represent strategic – that is, functional – ways of developing under different rearing conditions (Meaney, 2010).

A central premise of the ACM is that human children likewise have evolved to function competently – to survive and ultimately reproduce – in a variety of contexts; thus, our default assumption is that alternative patterns of stress responsivity and related variation in life history-related behavior, both in response to stressful and supportive environmental conditions (within the range encountered over human evolution), constitute adaptive developmental variation. Along these lines, an evolutionary–developmental perspective emphasizes conditional adaptation: “evolved mechanisms that detect and respond to specific features of childhood environments, features that have proven reliable over evolutionary time in predicting the nature of the social and physical world into which children will mature, and entrain developmental pathways that reliably matched those features during a species’ natural selective history” (Boyce and Ellis, 2005, p. 290; for a comprehensive treatment of conditional adaptation, see West-Eberhard, 2003). Conditional adaptation, which is closely related to the concept of a predictive adaptive response (e.g., Gluckman et al., 2007), is guided by both external environmental factors (e.g., predation pressures, quality of parental investment, seasonal change, and diet) and indicators of the individual's status or relative competitive abilities in the population (e.g., age, body size, health, history of wins and losses in agonistic encounters).

Boyce and Ellis (2005) have proposed a conditional adaptation model of developmental variation in the human SRS. This model articulated the precepts and rationale for a new claim about the nature of relations between early life experience and stress responsivity. Boyce and Ellis (2005) contend that heightened responsivity may reflect, not simply exaggerated arousal under challenge, but rather a form of enhanced, neurobiologically mediated sensitivity to context, or biological sensitivity to context (BSC).

The concept of BSC has its early roots in a 1995 Psychosomatic Medicine report by Boyce and colleagues (1995b), presenting two studies of naturally occurring environmental adversities and stress reactivity as predictors of respiratory illnesses in 3–5-year old children. Results revealed, first, that children showing low cardiovascular or immune reactivity to stressors had approximately equal rates of respiratory illnesses in both low and high adversity settings. Second, and consistent with the prevailing diathesis-stress model, highly biologically responsive children exposed to high adversity child care settings or home environments had substantially higher illness incidences than all other groups of children. The third, and unexpected, finding was that highly responsive children living in lower adversity conditions – i.e., more supportive child care or family settings – had the lowest illness rates, significantly lower than even low responsive children in comparable settings.

These data suggested that children differed in their susceptibility to environmental influence in a “for better and for worse” manner (Belsky et al., 2007), with more biologically responsive children experiencing unusually poor outcomes in high-stress, unsupportive social conditions but flourishing under low-stress, nurturing, and predictable conditions. Further, the initial Boyce et al. (1995b) research, together with subsequent work (Boyce and Ellis, 2005), identified candidate physiological mechanisms of environmental susceptibility – autonomic, adrenocortical, or immune reactivity to psychosocial stressors – and proposed that psychobiologic reactivity moderated the effects of early environmental exposures on physical and mental health outcomes in a bivalent manner. More responsive children displayed heightened sensitivity to both positive and negative environmental influences and thus were given the shorthand designation of orchid children, signifying their special susceptibility to both highly stressful and highly nurturing environments. Children low in responsivity, on the other hand, were designated as dandelion children, reflecting their relatively high capacity for survival in species-typical circumstances of all varieties (Boyce and Ellis, 2005).

Although the findings of Boyce et al. (1995b) stimulated a provisional interpretation of how environmental exposures and psychobiologic responsivity worked together in regulating children's mental and physical health, conspicuously missing was a broader, more heuristic theoretical framework in which these findings could be interpreted and explained. Boyce and Ellis's (2005; see also Ellis et al., 2005, Ellis et al., 2006, Ellis and Boyce, 2008) BSC theory was an effort to provide such an evolutionary functional analysis, advancing as it did two key propositions. The first involved a new hypothesis about the function of the SRS and the second a novel evolutionary hypothesis about its developmental calibration. Each is considered here, in turn.

With respect to the function of the SRS, it was clear that biological reactivity to stressors comprises a complex, integrated system of central neural and peripheral neuroendocrine responses designed to prepare the organism for challenge or threat. On the other hand, according to BSC theory, the components of the “stress response” system also function to increase susceptibility to resources and support in the environment. This dual function signifies the need to conceptualize stress responsivity more broadly as BSC, which Boyce and Ellis (2005) defined as neurobiological susceptibility to both cost-inflicting and benefit-conferring features of the environment and operationalized as an endophenotypic property indexed by heightened responsivity in one or more components of the SRS.

Highly responsive children experience either the best or the worst of psychiatric and biomedical outcomes within the populations from which they are drawn. Under conditions of adversity, such children sustain higher rates of disease, behavioral problems, and injuries than their more normatively reactive peers. By contrast, such highly responsive children in low-stress, protective social environments experience substantially lower rates of physical and mental health problems than their less reactive counterparts (Boyce, 1996, Boyce et al., 1995b, Bubier et al., 2009, Ellis et al., 2011b, Essex et al., 2011, Obradović et al., 2010, Obradović et al., 2011, Quas et al., 2004). BSC theory therefore posits that individual differences in the magnitude of biological stress responses function to regulate openness or susceptibility to environmental influences, ranging from harmful to protective. Complementing this perspective, Jay Belsky's theory of differential susceptibility also postulates that children, due to variation in temperament and genetics, differ in their susceptibility to both the adverse effects of risk-promoting early environments and the beneficial effects of development-enhancing rearing conditions (Belsky, 1997, Belsky, 2005, Belsky and Pluess, 2009).

The second evolutionary proposition of BSC, concerning developmental calibration of the SRS, draws on the concept of conditional adaptation. BSC theory proposed that humans have evolved developmental mechanisms for detecting and internally encoding information about levels of support versus adversity in early childhood environments; this information is then used to calibrate activation thresholds and response magnitudes within stress response systems to match those environments. Given past evidence that early trauma can increase stress responsivity and newer evidence that responsivity can enhance developmental functioning in highly supportive settings, Boyce and Ellis (2005) postulated a curvilinear, U-shaped relation between early support-adversity and the magnitude of biological response dispositions. Specifically, Boyce and Ellis hypothesized that: (a) exposure to acutely stressful childhood environments up-regulates BSC, increasing the capacity and tendency of individuals to detect and respond to environmental dangers and threats; (b) exposure to especially supportive childhood environments also up-regulates BSC, increasing susceptibility to social resources and ambient support; and (c) by contrast, exposure to childhood environments that are not extreme in either direction down-regulates BSC. Because development of heightened BSC has associated fitness costs (e.g., increased rates of mental and physical disorders; reviewed in Boyce and Ellis, 2005), enhanced neurobiological susceptibility to the environment is unlikely to be adaptive in the large majority of children who grow up in normative environments. Instead, low to normative levels of BSC should produce the best fitness outcomes in such contexts, buffering individuals against the chronic stressors encountered in a world that is neither highly threatening nor consistently safe. Exploratory analyses in two studies offered confirmatory evidence that the lowest prevalences of highly responsive phenotypes were found in conditions of moderate stress and that both tails of the support-adversity distribution were associated with higher proportions of responsive children (Ellis et al., 2005; see also Gunnar et al., 2009a, Hagan et al., 2010). Converging findings of a curvilinear relationship between early stress and later responsivity have also been reported in recent studies of mice (Macrì et al., 2007, Macrì et al., 2009).

The ACM extends and refines the original BSC theory in a number of ways. First of all, we explicitly connect the concept of sensitivity to context to the broader evolutionary framework of LH theory. Second, we discuss the adaptive meaning and developmental origin of sex differences in responsivity, a crucial aspect that was missing from the initial formulation of the BSC theory. Third, we attempt to model the trajectories leading to individual differences in a more fine-grained way, by discussing the development of stress responsivity at different life stages and identifying a number of “switch points” when plasticity is preferentially expressed. Finally, we refine the BSC construct of stress responsivity by considering distinct roles for the three main components of the SRS (the parasympathetic and sympathetic systems and the hypothalamic–pituitary–adrenal axis). This allows us to model four prototypical responsivity patterns, each reflecting the coordinated activity of the SRS components.

The paper is organized as follows. Section 2 introduces the basics of LH theory and describes the role of LH strategies in the organization of behavior. Section 3 presents the evolutionary view of human development as a sequence of stages and switch points, and discusses the main switch points in the development of LH strategies. Section 4 is a synthetic review of the biological functions fulfilled by the SRS—the coordination of the allostatic response, the encoding/filtering of environmental information, and the regulation of life history-relevant traits. In Sections 5 The Adaptive Calibration Model of stress responsivity, 6 Patterns of responsivity we present the Adaptive Calibration Model, describe four prototypical patterns of stress responsivity, and explore their developmental trajectories across life stages. We conclude with a theoretical integration and a discussion of current limitations and future directions.