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The assumption that early stress leads to dysregulation and impairment is widespread in developmental science and informs prevailing models (e.g., “toxic stress”). An alternative evolutionary-developmental approach, which complements the standard emphasis on dysregulation, proposes that early stress may prompt the development of costly but adaptive strategies that promote survival and reproduction in adverse conditions. Here we survey this growing theoretical and empirical literature, highlighting recent developments and outstanding questions. We review concepts of adaptive plasticity and conditional adaptation, introduce the life history framework and the Adaptive Calibration Model, and consider how physiological stress response systems and related neuroendocrine processes may function as plasticity mechanisms. We then address the evolution of individual differences in susceptibility to the environment, which engenders systematic person-environment interactions in the effects of stress on development. Finally, we discuss stress-mediated regulation of pubertal development as a case study of how an evolutionary-developmental approach can foster theoretical integration.
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Annual Review of Psychology
Developmental Adaptation to
Stress: An Evolutionary
Bruce J. Ellis1and Marco Del Giudice2
1Department of Psychology and Department of Anthropology, University of Utah, Salt Lake
City, Utah 84112, USA; email:
2Department of Psychology, University of New Mexico, Albuquerque, New Mexico 87131, USA
Annu. Rev. Psychol. 2019. 70:111–39
First published as a Review in Advance on
August 20, 2018
The Annual Review of Psychology is online at 122216-
Copyright c
2019 by Annual Reviews.
All rights reserved
developmental plasticity, developmental programming, differential
susceptibility, evolution, life history theory, puberty, childhood stress,
stress response systems
The assumption that early stress leads to dysregulation and impairment is
widespread in developmental science and informs prevailing models (e.g.,
toxic stress). An alternative evolutionary–developmental approach, which
complements the standard emphasis on dysregulation, proposes that early
stress may prompt the development of costly but adaptive strategies that pro-
mote survival and reproduction under adverse conditions. In this review, we
survey this growing theoretical and empirical literature, highlighting recent
developments and outstanding questions. We review concepts of adaptive
plasticity and conditional adaptation, introduce the life history framework
and the adaptive calibration model, and consider how physiological stress re-
sponse systems and related neuroendocrine processes may function as plas-
ticity mechanisms. We then address the evolution of individual differences
in susceptibility to the environment, which engenders systematic person–
environment interactions in the effects of stress on development. Finally,
we discuss stress-mediated regulation of pubertal development as a case
study of how an evolutionary–developmental approach can foster theoretical
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OVERVIEW...................................................................... 112
ANDCONDITIONALADAPTATION ....................................... 113
Life History Theory as a Framework for Adaptive Plasticity . . . . . . . . . . . . . . . . . . . . . . 115
OutstandingQuestions andChallenges.......................................... 116
AS MECHANISMS OF CONDITIONAL ADAPTATION . . . . . . . . . . . . . . . . . . . . . 117
The Adaptive Calibration Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118
Comparing the Adaptive Calibration Model and Allostatic Load Model . . . . . . . . . . . 120
OutstandingQuestions andChallenges.......................................... 122
TOTHE ENVIRONMENT................................................... 122
Models of Differential Susceptibility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123
Markers of Susceptibility . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
OutstandingQuestions andChallenges.......................................... 126
Timingof Puberty:ACase Study................................................ 127
An Evolutionary–Developmental Theory of Pubertal Variation . . . . . . . . . . . . . . . . . . . 128
Accelerated Pubertal Maturation Trades Off Against Health . . . . . . . . . . . . . . . . . . . . . . 129
Stress Response Systems as Mediating Mechanisms in Stress–Puberty Relations. . . . 129
Importance of Differential Susceptibility in Regulation of Pubertal Timing . . . . . . . . 130
CONCLUSION.................................................................. 131
A widespread assumption in developmental science is that children raised in supportive and well-
resourced environments (e.g., those who live in communities with social networks and resources
for young people, who have strong ties to schools and teachers, and who benefit from nurturing and
supportive parenting) tend to develop normally and express optimal trajectories and outcomes.
By contrast, children raised in high-stress environments (e.g., those who experience poverty,
discrimination, and community disorganization; who feel disconnected from teachers and schools;
and who experience high levels of family conflict) are at risk for developmental dysregulation,
leading to impaired functioning and problem behaviors that are destructive to themselves and
others. These assumptions are powerful and pervasive, if usually implicit, and underlie prominent
models of development that focus on dysregulation and pathology [e.g., models of cumulative
risk (Evans et al. 2013), toxic stress (Shonkoff et al. 2012), and allostatic load (Lupien et al. 2006,
McEwen & Stellar 1993)].
In this review, we survey a growing theoretical and empirical literature focused on the idea that
stressful environments may prompt the development of costly but potentially adaptive strategies.1
This evolutionary–developmental perspective suggests that at least some of the outcomes of early
1The term adaptive in biology refers strictly to reproductive fitness and does not imply that a trait is socially desirable or
conducive to well-being; this is discussed in greater detail below.
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adversity may represent not dysfunction, but rather biologically adaptive strategies for dealing
with adversity (e.g., Belsky et al. 1991, Ellis & Del Giudice 2014, Ellis et al. 2017a, Frankenhuis
et al. 2016b). This emphasis on developmental adaptation to stress complements the standard
emphasis on dysregulation and negative health consequences. We do not deny or downplay the
costs of adaptations to adversity, which may include risk for genuine pathology and dysregulation.
However, as a counterpoint to the nearly exclusive focus on pathology and dysregulation in the
developmental literature, we concentrate on the potential for adaptation. Our goal is to introduce
the reader to key ideas and findings, summarize the present state of knowledge, and consider some
of the challenges and outstanding questions that face researchers in this area.
In the next section, we review the concepts of developmental plasticity and conditional adapta-
tion, introducing life history theory as a useful framework to conceptualize the effects of early stress
across behavioral, physiological, and developmental phenotypes. Next we consider how stress re-
sponse systems and related neuroendocrine processes may function as mechanisms of plasticity,
collecting information about key aspects of the environment and translating it into broad patterns
of life history–relevant traits. We highlight the adaptive calibration model (ACM; Del Giudice
et al. 2011), a theory of adaptive individual differences in stress physiology that contrasts with
disease-focused models such as allostatic load and toxic stress. The next section addresses indi-
vidual differences in susceptibility to the environment. The effects of stress are moderated by
individual factors, giving rise to systematic person–environment interactions. We review the main
evolutionary models of differential susceptibility and discuss empirical research on the genetic,
physiological, and behavioral mediators of plasticity. Finally, in the section titled Beyond Frag-
mentation: Toward an Integrated Theory of Stress, Developmental Adaptation, and Health, we
use the example of timing of pubertal maturation to illustrate how biological embedding of early
adversity can both impair development and guide it in an adaptive manner by promoting survival
and reproduction under more harsh and unpredictable conditions, despite the attendant costs to
health and well-being. We conclude that it is necessary to understand developmental adaptations
to stress—the coherent, functional changes that occur in response to adversity—to understand
the costs associated with these adaptations (e.g., allostatic load and its consequences).
Theory and research in evolutionary biology have come to acknowledge that, in most species, a
single best strategy for survival and reproduction is unlikely to evolve. Instead, the locally optimal
strategy normally varies as a function of three overarching factors (see Ellis & Del Giudice 2014).
First, the costs and benefits of different strategies depend on the physical and social parameters of
an organism’s environment (e.g., food availability, mortality rates, quality of parental investment,
social competition). This context dependency means that a strategy that promotes success in some
environmental contexts may lead to failure in others. Second, the success and failure of different
strategies depend on an organism’s internal condition and competitive abilities relative to other
members of the population (e.g., age, body size, health, history of wins and losses in agonistic
encounters). Third, an organism’s sex often has important implications for the range of available
strategies and their relative costs and benefits.
Because the viability of different survival and reproductive strategies is context and con-
dition dependent, natural selection tends to favor adaptive developmental plasticity, whereby
evolved mechanisms reliably guide the development of alternative phenotypes (including anatomy,
physiology, and behavior) to match an organism’s internal condition and external environment
(see West-Eberhard 2003). Developmental plasticity involves “durable biological change in the Developmental Adaptation to Stress 113
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structure or function of a tissue, organ, or biological system” (Kuzawa & Quinn 2009, p. 132).
Importantly, adaptive developmental plasticity is a nonrandom process; it is the outcome of struc-
tured interplay between the organism and its environment, shaped by natural selection to increase
the capacity of individuals to track both their internal condition and their external environments
and, integrating this information, to adjust the development of their phenotypes accordingly.
The occurrence of developmental plasticity, which is ubiquitous in the animal world, is un-
controversial (for extensive reviews, see DeWitt & Scheiner 2004, West-Eberhard 2003). For
example, it is widely recognized that harsh developmental conditions, such as exposure to a sub-
optimal intrauterine environment, can induce durable biological changes in the phenotype (e.g.,
Conradt et al. 2018). The question is whether exposures to physical and psychosocial stressors
simply constrain development, as assumed in dysregulation models, or guide it in an adaptive
From an evolutionary perspective, developmental plasticity is critically important for enabling
organisms to adapt to stressful conditions. Stress and adversity have always been part of the
human experience. Indeed, almost half of children in hunter–gatherer societies—the best model
for human demographics before the agricultural revolution—die before reaching adulthood (e.g.,
Volk & Atkinson 2013). Thus, from an evolutionary–developmental perspective, stressful rearing
conditions, even if those conditions engender sustained stress responses that must be maintained
over time, should not so much impair neurobiological systems as direct or regulate them toward
patterns of functioning that are adaptive under stressful conditions (Ellis & Del Giudice 2014,
Ellis et al. 2012a).
Because adaptive developmental plasticity involves durable change, it is inherently forward
looking; that is, it involves predicting—and preparing—for future conditions (both internal and
external). Boyce & Ellis (2005, p. 290) make preparation for future environments explicit in their
definition of 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.” A similar emphasis on forward-looking adaptation (focusing on potential later
fitness advantages) is conveyed by the phrase predictive adaptive response, which is often used to
describe the long-lasting effects of prenatal nutrition, exposure to maternal stress hormones, and
other early environmental factors (Bateson et al. 2014). Predictive adaptive responses need to be
distinguished from immediate adaptive responses, a term that refers to phenotypic responses that
afford immediate adaptive benefits (as when a fetus accelerates parturition in the context of an
infected uterus) (Bateson et al. 2014).
Developmental plasticity necessitates developmental trade-offs. For example, tadpoles (Rana
sylvatica) alter their size and shape based on the presence of dragonfly larvae in their rearing
environment (Van Buskirk & Relyea 1998). These alterations involve development of smaller and
shorter bodies and deep tail fins. Although tadpoles that do not undergo these morphological
changes are highly vulnerable to predation by dragonflies, those that do but end up inhabiting
environments that are not shared with dragonflies have relatively poor developmental and survival
outcomes. In short, the predator-induced phenotype is only conditionally adaptive. This process
highlights the fact that, in many cases, natural selection favors a primary phenotype that yields
high payoffs under favorable circumstances and a secondary phenotype that makes the best of a
bad situation (West-Eberhard 2003). Adaptations to adversity often entail significant costs and
drawbacks, even when they enhance an individual’s survival and reproduction prospects.
A conditional adaptation perspective has been applied not only to the development of person-
ality traits such as aggression, impulsivity, and risk taking (e.g., Belsky et al. 1991, Daly & Wilson
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2005, Del Giudice 2015b, Ellis et al. 2012a), but also to cognitive abilities such as enhanced
stimulus-response learning and executive function components relevant to monitoring changes in
the environment (e.g., the ability to rapidly switch between tasks and update working memory)
(Mittal et al. 2015, Young et al. 2018; for a review, see Ellis et al. 2017a). Such cognitive traits can
be especially useful in unpredictable and fluctuating contexts.
Life History Theory as a Framework for Adaptive Plasticity
In evolutionary biology, a major framework for explaining coordinated patterns of developmen-
tal plasticity is life history theory (see Del Giudice et al. 2015, Ellis et al. 2009). Life history
theory addresses how organisms allocate their limited stocks of time and energy to the various
activities (including growth, maintenance of bodily tissues, mating, and parenting) that compose
their life cycle. Since all of these activities ultimately contribute to the organism’s fitness, devot-
ing time and energy to one will typically involve both benefits and costs, engendering trade-offs
between different fitness components. Natural selection favors organisms that schedule develop-
mental activities so as to optimize resource allocation. The resulting chain of resource-allocation
decisions—expressed in the development of an integrated suite of physiological and behavioral
traits—constitutes the individual’s life history strategy. An organism’s life history strategy coor-
dinates morphology, physiology, and behavior in ways that maximize expected fitness in a given
environment (Ellis et al. 2009).
The critical decisions involved in a life history strategy can be summarized by the fundamental
trade-offs between current and future reproduction, between quality and quantity of offspring,
and—in sexually reproducing species—between mating and parenting effort (see Del Giudice
et al. 2015). At the broadest level of analysis, life history–related traits covary along a dimension
of slow versus fast life history. Variation along the slow–fast continuum is observed both between
related species and between individuals of the same species ( Jeschke et al. 2008, R ´
eale et al.
2010). In humans, some individuals adopt slower strategies characterized by later reproductive
development (especially in girls) and delayed sexuality, preferences for stable pair bonds and high
investment in parenting, an orientation toward future outcomes, low impulsivity, and allocation
of resources toward enhancing long-term survival; others display faster strategies characterized
by the opposite pattern (Belsky 2012, Belsky et al. 1991, Del Giudice et al. 2015, Ellis et al. 2009,
Figueredo et al. 2006). Fast life history strategies are comparatively high risk, focusing on mating
opportunities (including more risky and aggressive behavior), reproducing at younger ages, and
producing a greater number of offspring with more variable outcomes. Trade-offs incurred by
faster strategies include reduced health, vitality, and longevity (as discussed in the section titled
Beyond Fragmentation: Toward an Integrated Theory of Stress, Developmental Adaptation, and
In most organisms, individual life histories are determined by a combination of genetic and
environmental factors and often exhibit a remarkable degree of developmental plasticity. Key
dimensions of the environment that regulate the development of life history strategies include en-
ergy availability, extrinsic morbidity–mortality, and predictability of environmental change (Del
Giudice et al. 2015, Ellis et al. 2009). Energetic resources—caloric intake, energy expenditures,
and related health conditions—set the baseline for many developmental processes. Energy scarcity
slows growth and delays sexual maturation and reproduction, resulting in slower life history strate-
gies. However, when bioenergetic resources are adequate to support growth and development,
cues to extrinsic morbidity–mortality and unpredictability generally promote faster strategies.
Extrinsic morbidity–mortality refers to external sources of disability and death that are rela-
tively insensitive to the adaptive decisions of the organism. Environmental cues indicating high Developmental Adaptation to Stress 115
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levels of extrinsic morbidity–mortality (e.g., exposures to violence, harsh child-rearing practices,
premature disability and death of other individuals in one’s local ecology) cause individuals to de-
velop faster life history strategies. Faster strategies in this context—a context that devalues future
reproduction—function to reduce the risk of disability or death prior to reproduction. Moreover,
high extrinsic morbidity–mortality means that investing in parental care has quickly diminishing
returns, which favors reduced parental investment and offspring quantity over quality. In research
on industrialized populations, extrinsic morbidity–mortality is often operationalized in terms of
socioeconomic adversity because of the relationship between poverty and higher levels of virtu-
ally all forms of morbidity and mortality. However, some studies have also collected measures
of local mortality rates, developmental exposures to death and injury, or perceived danger in the
environment (e.g., Chang & Lu 2018, Copping & Campbell 2015, Johns 2011).
In addition to extrinsic morbidity–mortality, environmental unpredictability also regulates
development of life history strategies. In terms of evolutionary selection pressures, environmental
unpredictability has been defined as variation in extrinsic morbidity–mortality (Ellis et al. 2009). In
terms of adaptively calibrating developmental strategies, cues to environmental unpredictability
have typically been operationalized as stochastic changes in ecological and familial conditions
(e.g., Belsky et al. 2012, Simpson et al. 2012). In environments that fluctuate unpredictably,
long-term investment in development of a slow life history strategy may not optimize fitness.
Individuals should instead detect and respond to signals of environmental unpredictability (e.g.,
erratic neighborhood conditions, frequent residential changes, fluctuating economic conditions,
changes in family composition) by adopting faster strategies.
Since danger and unpredictability are core defining features of stress, life history theory of-
fers integrative principles for making predictions about how early stress shapes the development
of multiple behavioral traits, as well as the associations of these traits with patterns of growth,
sexual maturation, metabolism, immunity, and other life history–related systems. The life his-
tory perspective has inspired developmental research on the links between familial and ecological
stress and later outcomes such as impulsivity and risk taking, pubertal maturation, sexual be-
havior, reproductive timing, and health (e.g., Belsky et al. 2012, 2015b; Brumbach et al. 2009;
Copping & Campbell 2015; James et al. 2012; Mell et al. 2018; Sheppard et al. 2016; Simpson
et al. 2012; Sung et al. 2016; Szepsenwol et al. 2015). This work has been especially important
in advancing our understanding of the key distinction between childhood exposures to extrinsic
morbidity–mortality cues and environmental unpredictability (Ellis et al. 2009), each of which has
been found to uniquely predict the development of life history–related traits and associated health
Outstanding Questions and Challenges
The biological concept of plasticity, when applied to human development, brings with it some
important insights but also many complex problems and questions. For example, standard models
of plasticity assume that early stress carries predictive information about the future state of the en-
vironment (e.g., danger and consequent high mortality). An alternative (though not incompatible)
possibility is that early stress inflicts irreparable damage to the developing organism; in this view,
plasticity mechanisms respond to the individual’s compromised internal state and not to hypothet-
ical cues about its future environment (Rickard et al. 2014). Distinguishing between external and
internal (or somatic state–based) accounts of plasticity is going to require much careful empirical
work, as well as more refined theoretical models than are currently available (see Del Giudice
2014a, Hartman et al. 2017). Other important questions concern specific sensitive periods for the
effects of early stress and their evolutionary logic. The idea that the period from conception to
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the end of early childhood (i.e., the first 5–7 years of life) is especially critical is widespread in the
literature. However, the duration of sensitive windows may itself depend on earlier experiences
(Fawcett & Frankenhuis 2015); moreover, a long-lived species like ours may be characterized by
multiple windows of plasticity, including key developmental transitions such as the beginning of
middle childhood and the onset of puberty (see Del Giudice 2014b, Del Giudice & Belsky 2011,
Ellis 2013, Shulman et al. 2016).
Developmental research based on life history concepts faces similar challenges. There is still
much that we do not know about life history strategies, especially when moving from consider-
ing evolution within a population (the standard focus of biological models) to considering de-
velopment within a single individual (see Mathot & Frankenhuis 2018). Mathematical models
of life history evolution also raise the possibility that some long-term outcomes of early stress
are the legacy of immediate adaptive responses for infant survival, rather than adult adapta-
tions for mating and reproduction (i.e., predictive adaptive responses; see Wells & Johnstone
2017). Within evolutionary psychology, there is a lively ongoing debate about the best way to
measure life history–related behavioral traits and integrate them with demographic traits such
as puberty and reproductive timing (e.g., Black et al. 2017, Richardson et al. 2017). The in-
ferences that can be drawn from human research are also limited by the widespread lack of
control for potential genetic confounding in developmental studies that correlate early envi-
ronmental variables with later outcomes (see Barbaro et al. 2017). The problem of genetic con-
founding has been addressed in a minority of studies (e.g., Ellis et al. 2012b, Tither & Ellis
2008); fortunately, more researchers are starting to explicitly incorporate genetic information (e.g.,
Gaydosh et al. 2018), and the results will undoubtedly prompt revisions and refinements of current
How does repeated or chronic childhood adversity shape biobehavioral development and, through
it, mental and physical health? There is widespread agreement in the developmental literature
that early life adversities (both prenatal and postnatal) can cause enduring changes in biological
and developmental systems (i.e., biological embedding) that affect health and behavior over the
life course (e.g., Hertzman 2012). Controversy exists, however, regarding the functional versus
dysfunctional role of biological embedding in regulating (or dysregulating) the development of
the phenotype.
In developmental models that are primarily focused on explaining dysregulation, such as mod-
els of toxic stress (Shonkoff et al. 2012) and allostatic load (Lupien et al. 2006, McEwen &
Stellar 1993), biological embedding is construed negatively. These models postulate that biolog-
ical responses to stress are usually beneficial in the short term (i.e., that they facilitate immediate
adaptive responses), but protracted activation of stress responsive systems is maladaptive and toxic
in the long term. From this perspective, biological embedding of early life stress causes disruptions
of brain structure and function, resulting in dysregulation of physiological mediators—autonomic,
neuroendocrine, metabolic, and immune—that are “the precursors of later impairments in learning
and behavior as well as the roots of chronic, stress-related physical and mental illness” (Shonkoff
et al. 2012, p. e236). As eloquently stated by Juster and colleagues (2011, p. 725), the wear and
tear of toxic stress and altered stress hormone functioning “inexorably strains interconnected
biomarkers that eventually collapse like domino pieces trailing toward stress-related endpoints.”
Allostatic load is a term used to describe the wear and tear that results from repeated allo-
static adjustments (i.e., adaptation to stressors), which expose one to adverse health consequences Developmental Adaptation to Stress 117
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that increase as a person ages. According to the allostatic load model (ALM), there is an optimal
level of stress responsivity, and both hyper- and hypo-activation of physiological mediators are
routinely described as dysfunctional deviations from the norm, usually caused by a combination
of excessive stress exposure and genetic or epigenetic vulnerability. In this framework, develop-
mental stress exposures are regarded as risk factors for a wide array of symptoms and disorders.
While some authors have argued that optimal adaptation is fostered by environments that con-
tain moderate amounts of stressors (e.g., Rutter 1993), the underlying assumption remains that
a single best environment exists, and that deviations from that optimum cause dysregulation and
Accepting these assumptions without placing them in a larger evolutionary–developmental
framework has likely impeded our understanding of the role of stress response systems in adap-
tively regulating development (see Ellis & Del Giudice 2014). Specifically, models of allostatic
load focus on the long-term costs of childhood stress and adversity—the wear and tear on multiple
organ systems induced by chronic stress—but do not address the benefits of calibrating autonomic,
neuroendocrine, metabolic, and immune systems to match current and future environments (i.e.,
predictive adaptive responses). We argue that this overemphasis on costs misses something fun-
damental about developmental adaptation to stress and thus weakens the conceptual power of the
ALM. The result has been an imbalanced approach to research that has yielded dramatically more
empirical knowledge about dysfunction than about adaptive function, making it difficult to gain a
coherent big picture of the subject matter.
The Adaptive Calibration Model
A promising alternative to the ALM is provided by the ACM (Del Giudice et al. 2011), a theory of
individual differences in stress responsivity that builds on the concepts of life history theory and
developmental plasticity. The ACM supplements the ALM and revises some of its key assumptions,
thus laying the foundation for a broad theory of individual differences (for a more extended
discussion, see Ellis & Del Giudice 2014). The central tenet of the ACM is that physiological
stress response systems, including the autonomic nervous system and the hypothalamic–pituitary–
adrenal (HPA) axis, operate as mechanisms of conditional adaptation, with a key role in regulating
the development of individual life history strategies.
In the ACM, the activation of autonomic and adrenocortical responses during childhood pro-
vides crucial information about threats and opportunities in the environment, their type, and their
severity. Over time, this information becomes embedded in the parameters—recurring set points
and reactivity patterns—of these physiological systems, which in turn provide the developing
person with statistical summaries of key dimensions of the environment. For example, sustained
activation of the HPA axis is generated by exposures to danger, unpredictable or uncontrollable
contexts, and social evaluation, as well as by energetic stress (Dickerson & Kemeny 2004); thus, the
HPA axis tracks the key environmental variables involved in regulation of alternative life history
strategies. In turn, individual differences in the functioning of stress response systems regulate the
coordinated development of a broad cluster of life history–related physiological and psychological
traits, including growth and maturation, sexual and reproductive functioning, social learning, ag-
gression, competition and risk taking, pair bonding, and related factors (Del Giudice et al. 2011,
Ellis & Del Giudice 2014). Other systems that contribute to life history regulation include the
hypothalamic–pituitary–gonadal axis; the serotonergic, dopaminergic, and oxytocinergic systems;
and the immune system (discussed in more detail below). Not coincidentally, all of these sys-
tems engage in extensive bidirectional cross talk with stress response systems (for reviews, see Del
Giudice et al. 2011, Ellis & Del Giudice 2014).
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Patterns of stress responsivity. In contrast to the notion of a single optimal stress responsivity
pattern (as per the ALM), the ACM proposes that two different adaptive patterns of stress re-
sponsivity emerge in the context of high childhood adversity. The first pattern, labeled vigilant, is
characterized by heightened physiological stress reactivity (across the sympathetic nervous system
and HPA axis) and is predicted to develop in dangerous or unpredictable contexts, where it enables
people to cope with threats in their physical and social environment. In the ACM, the vigilant
profile mediates heightened vigilance and attention to threats; it is associated with elevated lev-
els of anxious and depressed behaviors (especially in females) and increased risk taking, agonistic
social competition, and reactive aggression (especially in males), consistent with a fast life history
strategy. The second pattern, labeled unemotional, is characterized by low physiological stress
reactivity across autonomic and adrenocortical systems and is predicted to develop under condi-
tions of severe, chronic stress. According to the ACM, generalized unresponsivity in this context
inhibits sensitivity to social feedback and can increase risk taking by blocking information about
dangers and threats in the environment (e.g., leading to low anxiety). In line with a fast life history
strategy, the unemotional profile is associated with low empathy and cooperation, impulsivity,
competitive risk taking, and antisocial behavior, including high levels of proactive and instrumen-
tal aggression, especially in males. The hypothesized vigilant and unemotional profiles, reflecting
the emergence of both high and low stress responsivity patterns in the context of adversity, have
been documented in longitudinal studies of Dutch adolescent males (Ellis et al. 2017c) and chil-
dren in the United States (Laurent et al. 2014), although with some deviations from expected
patterns (for a discussion, see Ellis et al. 2017b).
More generally, psychosocial stress and adversity over the course of development can either
upregulate or downregulate levels of autonomic and adrenocortical reactivity. The empirical lit-
erature on this topic remains conflicted. On the one hand, many studies link stressful rearing
experiences to hyper-reactivity, supporting the vigilant responsivity pattern; on the other hand,
an equally impressive number of studies link stressful rearing experiences to hypo-reactivity, sup-
porting an unemotional responsivity pattern (for reviews, see Del Giudice et al. 2011, Ellis et al.
2017b). In the ACM, we proposed that some children who grow up under high-stress conditions
will first develop high stress responsivity in early childhood (vigilant profile), then shift to low
responsivity during juvenility or adolescence (unemotional profile) as social competition becomes
a central developmental task. We also hypothesized that this trajectory would be more common
in males (Del Giudice et al. 2011). A shift from hyper- to hypo-reactivity may help to explain an
otherwise puzzling finding in the literature: that the overall association between basal cortisol lev-
els and aggressive/externalizing behavior tends to be positive in preschoolers but negative starting
from middle childhood (Alink et al. 2008).
The proposed developmental transition from a vigilant to an unemotional profile has been
demonstrated in longitudinal studies of individuals with a history of child maltreatment. Doom
et al. (2014) reported that such individuals transitioned from initially high levels of basal afternoon
cortisol to blunted levels in middle childhood. Likewise, Trickett et al. (2010) found that females
with a history of child sexual abuse transitioned across development from initially elevated levels
of morning cortisol to attenuated levels starting in adolescence, whereas females who were not
sexually abused maintained similar normative morning cortisol levels across development. Con-
sistent with the unemotional responsivity pattern, youth exposed to maltreatment also display
blunted cortisol reactivity by early adolescence, and this effect tends to be stronger in boys than
in girls when contrasting maltreated and comparison groups (see Trickett et al. 2014, figure 2). A
similar sex-specific effect was found in a recent study in South Africa: Adverse childhood experi-
ences predicted blunted cortisol reactivity in boys but increased reactivity in girls (Fearon et al.
2017). Developmental Adaptation to Stress 119
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The hypothesized developmental transition from a vigilant to an unemotional profile converges
with the well-established pattern of HPA responses to chronic stress: Initially, stressors tend to
acutely upregulate basal cortisol levels in the time period proximal to stressor onset; however,
over time, severe chronic stress exposures tend to downregulate hormonal output and elicit a flat
diurnal cortisol rhythm (for a meta-analysis, see Miller et al. 2007). Extending these findings on
basal cortisol activation, a meta-analysis of cortisol responsivity to social stress (Bunea et al. 2017)
found that early life adversity was robustly associated with blunted cortisol reactivity in adults
(large effect) but not in children and adolescents (small effect). Given the focus of this meta-
analysis on adverse childhood experiences that were typically chronic and severe, the results are
consistent with the ACM’s proposed developmental transition to an unemotional profile under
high-stress conditions.
Extending the adaptive calibration model: adaptive calibration of the immune system.
Another mechanism through which childhood adversity may promote faster life history strategies
is through calibration of immune system parameters. As reviewed by Nusslock & Miller (2016),
childhood stress exposures sensitize cortico-amygdala neural circuitry in a manner that enhances
vigilance and threat processing, and they alter the activity of immune cells in a manner that
promotes and sustains inflammation. For example, greater family stress, trauma, and adversity are
associated with heightened amygdala reactivity to negative emotional stimuli (e.g., Herringa et al.
2016), higher concentration of inflammation-related molecules (e.g., Baumeister et al. 2016), and
profiles of gene expression consistent with a proinflammatory phenotype (e.g., Robles et al. 2018).
Nusslock & Miller (2016, p. 25) proposed that cortico-amygdala threat circuitry and immune
cells that propagate inflammation are “components of an integrated, bidirectional network that
detects threats to well-being and mobilizes behavioral, physiologic, and inflammatory resources
for coping.” Most importantly, cross talk between these two components appears to be potentiated
by early adversity. Nusslock & Miller (2016) conceptualized this enhanced cross talk as promoting
immediate adaptive responses to danger, as when brain-to-immune signaling readies the immune
system for pathogen eradication and tissue healing, or when immune-to-brain signaling enhances
threat vigilance. In the long run, these processes may contribute to the pathogenesis of emotional
and physical health problems.
The relationship between immune functioning and life history strategies is most likely bidi-
rectional. Like stress response systems, the immune system collects and relays information about
important sources of danger and mortality, specifically the prevalence and type of pathogens in the
local environment and the individual’s ability to effectively cope with them. Thus, early immune
activity should contribute to the development of alternative life history strategies (e.g., Hill et al.
2016, Kopp & Medzhitov 2009). At the same time, different life history strategies can be expected
to entail different patterns of investment in immune defenses. For example, researchers have be-
gun to examine the possibility that faster life history strategies may predict increased investment
in innate immunity (including inflammation) at the expense of acquired immunity (Georgiev et al.
Comparing the Adaptive Calibration Model and Allostatic Load Model
The ACM and ALM diverge considerably in how they deal with cost–benefit trade-offs, individual
differences, and long-term developmental changes.
Different views of cost–benefit trade-offs in development. In an evolutionary framework, the
terms adaptive and maladaptive denote the effect of a trait or behavior on biological fitness. From
120 Ellis ·Del Giudice
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the standpoint of the individual organism, adaptive traits are those that enhance its expected fitness
more than do potential alternatives. However, all adaptations have fitness costs as well as benefits;
to be adaptive, a trait does not have to be cost free, but only to yield a positive overall contribution
to fitness. This notion of adaptation and maladaptation contrasts sharply with how the same terms
are usually employed in health- and disease-focused disciplines, wherein adaptive refers to traits
and behaviors that are socially desirable (e.g., that promote health, safety, subjective well-being,
and mutually rewarding social relations), while maladaptive refers to traits and behaviors that are
socially undesirable (e.g., that have aversive or health-damaging effects).
The ALM makes no distinction between these two meanings of adaptive and maladaptive.
Indeed, maladaptation is typically inferred whenever there are substantial costs to the organism.
For example, if elevated cortisol levels in adolescents are associated with an undesirable outcome,
such as reduced working memory, then elevated cortisol is deemed maladaptive (and classified
as a biomarker of allostatic load) (see Juster et al. 2011). This reasoning ignores the crucial fact
that biological processes are maintained by natural selection when their fitness benefits outweigh
the costs, not when they are cost free; indeed, even large costs can be offset by large enough
expected benefits. Because of the failure to distinguish between (mal)adaptive and (un)desirable
outcomes, most applications of the ALM do not adequately address the trade-offs involved in the
development of physiological and behavioral phenotypes; as a consequence, the ALM literature
often lacks a theory of adaptive individual variation in stress responsivity. In the ALM, the focus
is on optimal parameter values of stress response systems, as defined by covariation with desirable
health outcomes; deviations from these optimal settings form the basis of dysregulation.
In contrast, the ACM emphasizes adaptation in context and posits that optimal stress response
parameters vary as a function of environmental conditions, as illustrated by the vigilant and un-
emotional responsivity patterns. From this perspective, the notion of globally optimal responsivity
levels is problematic. For example, consider heightened stress responsivity in dangerous, unpre-
dictable environments (as in the vigilant pattern). In the ACM, it is hypothesized that the costs of
repeated stress system activation are offset by improved management of danger (Del Giudice et al.
2011). Although the system is on a hair trigger, with a resulting increase in anxiety or aggression,
few instances of actual danger will be missed. In addition, engaging in a fast, present-oriented
life history strategy makes it optimal to discount the long-term health costs of chronic activation
of stress response systems if the immediate benefits are large enough. In the ALM framework,
the same pattern of responsivity would be treated as dysfunctional because the stress response is
deployed even in the absence of true dangers (resulting, for example, in excessive responding or
unnecessary triggering) (e.g., Lupien et al. 2006) and because of the associated undesirable states
and health risks (e.g., anxiety, increased cardiovascular risk).
Different views of long-term adaptations to stress. According to the ACM, childhood adap-
tations to stress may eventuate in long-term adaptive changes in biobehavioral systems. Herein
lies the key difference between the ACM and ALM. In the ALM, energy devoted to mount-
ing autonomic, neuroendocrine, metabolic, and immune responses to threat (immediate adaptive
responses) is traded off against wear and tear on multiple organ systems. This wear and tear,
according to the ALM, results in dysfunctional changes in the regulatory parameters of stress re-
sponse systems (i.e., dysregulation). These biologically embedded changes are commonly viewed
as indicators of allostatic load, reflecting the costs of stress-induced trade-offs; they are explicitly
not viewed as predictive adaptive responses. By contrast, the ACM conceptualizes these trade-offs
as decision nodes in allocation of resources. Through biological embedding, each decision node
influences the next (opening up some options, foreclosing others), thus progressively favoring one
developmental trajectory over another. Predictive adaptive responses are instantiated through this Developmental Adaptation to Stress 121
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chain of resource-allocation decisions, which calibrates the developing phenotype to current (and
expected future) conditions. In total, the ACM shifts the emphasis from dysregulation to condi-
tional adaptation. From this perspective, development of a fast life history strategy in dangerous
and unpredictable contexts is not impairment or dysfunction; it is a coherent, organized response
to stress that has been shaped by a natural selective history of recurring exposures to such contexts
(for a detailed human example, see the section titled Beyond Fragmentation: Toward an Integrated
Theory of Stress, Developmental Adaptation, and Health).
Outstanding Questions and Challenges
The ACM and ALM offer sharply different perspectives on the costs and benefits of adaptations
to stress, particularly in regard to long-term developmental trajectories. The most urgent task
for researchers is to design studies capable of distinguishing between the two models. At present,
studies based on the ALM focus solely on the costs of childhood adversities (allostatic load) and
do not even attempt to explore the potential benefits of the attendant physiological and behavioral
changes (adaptive calibration). As an initial step in this direction, Del Giudice et al. (2011) made
specific hypotheses about how different environmental conditions should give rise to adaptive
profiles of stress responsivity, growth and maturation, and behavior. Some predictions have been
supported—for example, both high- and low-responsivity patterns have been identified in safe
as well as harsh conditions (e.g., Del Giudice et al. 2012; Ellis et al. 2005, 2017c; Fearon et al.
2017; Gunnar et al. 2009). Other predictions (for example those concerning sex differences in
high- versus low-responsivity profiles) have received mixed support, while others still are in need
of revision (see Ellis et al. 2017b). This is to be expected, since moving from the general principles
reviewed in this article to empirical predictions requires many additional assumptions about the
functions and correlates of particular physiological variables.
As discussed above, another important task will be to extend the ACM to include metabolism
and immunity, two key domains that have received considerable attention in the ALM framework.
The ultimate goal should be to build a detailed map of how biologically embedded changes regulate
developmental adaptations to stress, from maturation and reproductive functioning to learning
and behavior. By delineating intervening functional changes that mediate the effects of early
adversity on later mental and physical health problems, such a map could transform research on
stress–health relations.
Finally, an adaptive calibration perspective raises methodological and statistical challenges that
have yet to be adequately addressed. Notably, ACM responsivity profiles combine stress physiology
with a range of other life history–related traits. Analyses that focus exclusively on the parameters of
stress response systems (e.g., autonomic reactivity, cortisol levels) are unlikely to recover function-
ally meaningful patterns (for an example of this issue, see Peckins et al. 2015). However, properly
combining behavioral, developmental, and physiological variables is a challenging task that will
require sophisticated statistical approaches (see Ellis et al. 2017b,c).
What makes developmental plasticity potentially adaptive is that it can match the organism’s phe-
notype to its environment (or internal condition) in ways that improve the organism’s capacity
for survival and reproduction (West-Eberhard 2003). We note above that plasticity is rarely with-
out costs; these include the costs and trade-offs involved in producing the appropriate phenotype
(e.g., adaptations to predators in tadpoles), but also the extra time spent sampling the environment
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before specializing. Moreover, the cues received from the environment are usually imperfect and
can lead to incorrect predictions; as a result, plastic organisms sometimes end up developing a
mismatched phenotype that decreases their fitness instead of enhancing it (e.g., a predator-adapted
phenotype when actual predation risk is low) (see Frankenhuis & Panchanathan 2011, Murren
et al. 2015).
For all these reasons, plasticity is not always the optimal strategy for organisms. This creates
the potential for the evolution of individual differences in plasticity: Within the same population,
some individuals may respond strongly to their rearing conditions, while others may be barely
affected (Belsky & Pluess 2009, Boyce & Ellis 2005, Ellis et al. 2011a). These differences have
important implications for studying the effects of stress on development: If conditional adaptation
is not a universal strategy, then the predicted correlations between early adversity and subsequent
trajectories will be significantly attenuated by individual variation in plasticity. Biological models
typically assume that individual differences in plasticity are determined by differences in genotype.
Another possibility is that early environmental factors also shape plasticity to later aspects of the
environment; for example, prenatal exposure to maternal stress hormones may modulate the child’s
sensitivity to the quality of parenting and family relations (Boyce & Ellis 2005, Conradt et al. 2018,
Del Giudice 2015a, Pluess & Belsky 2011). In this scenario, early stress and adversity play a dual
role—they work as cues for plasticity mechanisms, but also modulate the sensitivity of the same
mechanisms over time (Boyce & Ellis 2005).
The notion that some individuals are especially vulnerable to negative or stressful experiences
is not new, as exemplified by the classic developmental concept of diathesis stress. However,
standard vulnerability models focus exclusively on negative outcomes and lack a functional theory
of individual differences that explains why such differences may evolve and persist in a population.
This focus has changed with the rise of differential susceptibility models over the past 20 years
(Belsky 1997, 2005; Boyce & Ellis 2005; Boyce et al. 1995; Ellis et al. 2006, 2011a). According
to these models (reviewed below), many of the same factors that determine increased sensitivity
to stress and adversity may also confer enhanced responsivity to the positive, supportive aspects
of the environment. In other words, highly susceptible individuals respond to the quality of their
environment for better and for worse (Belsky et al. 2007, Boyce et al. 1995).
Models of Differential Susceptibility
Models of differential susceptibility are based on the idea that adaptive plasticity has costs and
potential drawbacks; they postulate the existence of individual differences in plasticity that give rise
to systematic person–environment interactions. At the same time, different models conceptualize
the costs of plasticity in somewhat different terms and propose alternative mechanisms for the
development of individual differences (see Belsky & Pluess 2016, Del Giudice 2016, Ellis et al.
Differential susceptibility theory. According to differential susceptibility theory (Belsky 1997,
2005), the biological function of differential susceptibility is to limit the evolutionary costs of plas-
ticity by making some individuals resistant to environmental influences, including those exerted
by parents. In other words, the theory predicts the existence of differences in susceptibility as a
form of insurance against developmental errors and mismatches. Indeed, mathematical models
show that individual differences in plasticity among siblings spread the risk of mismatch (a pattern
called bet hedging in evolutionary biology) and can be favored by natural selection in response to
unpredictable fluctuations in the environment (provided that other fairly restrictive assumptions
are met) (see Frankenhuis et al. 2016a). In Belsky’s (1997, 2005) original formulation, plasticity Developmental Adaptation to Stress 123
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was assumed to be essentially a function of genetic factors. Following biological sensitivity to
context theory (see below), the model was later expanded to include both genetic and early en-
vironmental effects (such as prenatal exposure to maternal stress hormones) as factors regulating
the development of differential susceptibility (Belsky & Pluess 2016, Pluess & Belsky 2011).
Biological sensitivity to context. The biological sensitivity to context model (Boyce & Ellis
2005; Ellis et al. 2005, 2006) is rooted in developmental research on health and adversity. Boyce
and colleagues (1995) found that children high in cardiovascular and immune reactivity have worse
health outcomes in stressful environments but better outcomes in positive and supportive environ-
ments. Boyce & Ellis (2005) reframed these findings in an evolutionary framework and developed
the biological sensitivity to context model. According to this model, differential susceptibility to
the environment is primarily mediated by individual differences in neurobiological traits, specifi-
cally variation in autonomic and adrenocortical reactivity to stress. This mechanistic focus is a key
distinguishing feature of the biological sensitivity to context model (and provided the conceptual
framework for the ACM responsivity patterns discussed above).
From an evolutionary standpoint, the biological sensitivity to context model links individual
differences in susceptibility to the coexistence of generalist phenotypes (low biological sensitivity
to context; metaphorically referred to as dandelions) and specialist phenotypes (high biological
sensitivity to context; metaphorically referred to as orchids). Whereas generalists do reasonably
well in most environments, specialists calibrate development to achieve high fitness in some kinds
of environments (e.g., dangerous and unpredictable ones) but not in others. A distinctive prediction
of the biological sensitivity to context model is that of a U-shaped curvilinear relationship between
early adversity and stress responsivity: Children growing up in very safe or very stressful conditions
should develop the highest susceptibility to environmental influences (and, as a result, become
specialized to their particular niche). This prediction has received some empirical support in
human developmental research (e.g., Del Giudice et al. 2012; Ellis et al. 2005, 2017c; Gunnar
et al. 2009). The hypothesized U-shaped curve is also consistent with simulations suggesting
that, in the presence of person–environment interactions such as those postulated by differential
susceptibility models, it may be optimal to express higher levels of plasticity at both ends of an
environmental continuum (Del Giudice 2015a).
Patterns of person–environment interaction. A notable contribution of differential suscepti-
bility models has been to direct the attention of researchers to the shape of person–environment
interactions. In the classic diathesis stress scenario, vulnerable and resilient individuals develop
in similar ways when they are exposed to favorable conditions but diverge at increasing levels of
stress and adversity. In contrast, models of differential susceptibility predict that high- and low-
susceptibility individuals should diverge in both safe and stressful conditions and only become
similar when they experience moderate levels of adversity (crossover interactions) (see Ellis et al.
2011a). More recently, Pluess & Belsky (2013) proposed that some individuals may exhibit vantage
sensitivity, a pattern symmetrical to that of diathesis stress whereby plasticity is only expressed in
safe, supportive environments. In both the diathesis stress and differential susceptibility scenarios,
adaptations to stress (e.g., risk taking, heightened or blunted HPA reactivity, altered immune
parameters) are expected to develop more reliably in highly susceptible individuals (so that the
overall effects of stress are attenuated by individual variation in susceptibility). Under the vantage
sensitivity scenario, however, adaptations to stress—to the extent that they occur—are expressed
uniformly by all individuals in the population. Devising methods to reliably distinguish among
these three interaction patterns has become the focus of a growing methodological literature (e.g.,
Belsky et al. 2013, Roisman et al. 2012).
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While most research in this area has been descriptive, the possibility that person–environment
interactions may fall into qualitatively different patterns raises a deeper question, namely, what
conditions can be expected to favor the evolution or development of each pattern (e.g., Pluess
2015). For example, initial mathematical models indicate that interaction patterns resembling the
classic diathesis stress template should evolve more frequently than patterns of vantage sensitivity,
unless negative states of the environment (stress, adversity) occur much more often than positive
ones (Del Giudice 2017a). The prediction that vantage sensitivity should be comparatively rare is
consistent with the fact that this pattern has only been detected in a small minority of studies (for
Markers of Susceptibility
What makes some individuals more susceptible than others to environmental influences, including
exposure to stress and adversity? More specifically, are there traits or markers that systematically
predict enhanced plasticity? To summarize the state of this very active area of research, we dis-
tinguish between three levels of analysis: genetics, physiology, and behavior (see also Belsky &
Pluess 2009, 2016).
Genetic markers. In the search for genetic markers of susceptibility, researchers have tested
genotype–environment (G ×E) interactions between particular genetic variants and observed en-
vironmental variables, such as parenting quality (correlational G ×E), or between genetic variants
and exposure to randomized conditions or treatments, such as interventions to reduce aggression
(experimental G ×E). Studies of single candidate genes have focused mainly on genes involved in
serotonergic and dopaminergic signaling, such as the dopamine receptor 4 gene (DRD4) or the
serotonin transporter gene (SLC6A4). Less often, researchers have considered genes with roles in
oxytocinergic signaling [e.g., the oxytocin receptor gene (OXTR)], the HPA axis [e.g., the corti-
cotropin releasing factor receptor 1 gene (CRHR1)], and other brain-related pathways [e.g., the
brain-derived neurotrophic factor (BDNF)] (see Belsky & Pluess 2016, Del Giudice 2017a, Moore
& Depue 2016).
The findings of individual studies in this area are highly variable (e.g., Belsky et al. 2015a)
and likely inflated by a high rate of false positives, as is typical of candidate gene studies (Dick
et al. 2015). So far, the most promising results come from meta-analyses of correlational G ×E
studies of dopaminergic and serotonergic genes (Bakermans-Kranenburg & van IJzendoorn 2011,
van IJzendoorn et al. 2012) and from more recent meta-analyses of experimental G ×E studies
involving the same genes (Bakermans-Kranenburg & van IJzendoorn 2015, van IJzendoorn &
Bakermans-Kranenburg 2015). It remains to be seen whether these results will be consistently
replicated in large samples. Another strategy to deal with the low statistical power of single-gene
studies is to pool multiple variants together into a polygenic score. Several studies employing
polygenic scores of serotonergic, dopaminergic, HPA-related, and other genes (such as BDNF)
have detected significant G ×E interactions, generally consistent with differential susceptibility
patterns (e.g., Belsky & Beaver 2011, Cicchetti & Rogosh 2012, Feurer et al. 2017, Keers & Pluess
2017, Silveira et al. 2017).
Physiological markers. According to the biological sensitivity to context model, a key marker
of susceptibility is elevated physiological reactivity to environmental challenges, including both
autonomic and HPA axis reactivity (Boyce & Ellis 2005, Ellis et al. 2005). Many empirical studies
have found patterns consistent with this idea (for reviews, see Boyce 2016, Obradovi´
c 2012),
although there are also contradictory findings (see Sijtsema et al. 2013). Importantly, there is
emerging evidence that stress reactivity itself may be the product of G ×E interactions between
early adversity and plasticity-enhancing genetic variants, in line with the hypothesis that initial Developmental Adaptation to Stress 125
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environmental cues modulate susceptibility to later experiences, particularly in individuals who are
already genetically plastic (Allegrini et al. 2018). More recently, Del Giudice and colleagues (2018)
speculated that exposure to higher levels of androgens (e.g., testosterone) during prenatal and
early postnatal life should increase plasticity for the many physiological and behavioral traits that
show higher variability in males. This hypothesis is still awaiting empirical testing; if supported,
it would extend the range of differential susceptibility markers beyond the typical emphasis on
central neurotransmitters and stress physiology.
Behavioral markers. In the foundational papers of differential susceptibility theory, Belsky (1997,
2005) suggested that behavioral traits such as difficult temperament and negative emotionality may
serve as markers of differential susceptibility in infants and children. This hypothesis has subse-
quently been tested in dozens of studies (see Belsky & Pluess 2016); a recent meta-analysis con-
firmed that difficult temperament and early negative emotionality (before 1 year of age) moderate
the effects of quality of parenting on child development in a way consistent with differential sus-
ceptibility (Slagt et al. 2016). Other researchers have pointed to sensory processing sensitivity as a
plausible marker of susceptibility (Boyce & Ellis 2005, Pluess 2015, Pluess et al. 2018). People high
in sensory processing sensitivity show heightened awareness of sensory stimulation, susceptibility
to overstimulation, elevated emotional reactivity (including both positive and negative emotion-
ality), and behavioral inhibition in novel situations (Aron et al. 2012). From a neurobiological
perspective, Moore & Depue (2016) argued that individual differences in the activity of multiple
brain systems (including dopaminergic, serotonergic, and oxytocinergic pathways) contribute to a
general dimension of reactivity to external stimulation, which may in turn determine susceptibility.
This neurobiological framework fits with the idea that susceptibility is, at least in part, a function
of the individual’s sensitivity to environmental stimuli, as reflected, for example, in measures of
sensory processing sensitivity (Pluess 2015). Initial results support a role for sensory processing
sensitivity in moderating some associations between parenting and externalizing behavior (Slagt
et al. 2018); however, there is still little empirical evidence that this trait is a general marker of
susceptibility, as has often been suggested in the literature (e.g., Pluess et al. 2018).
Outstanding Questions and Challenges
The study of differential susceptibility faces some formidable methodological challenges. Reli-
ably distinguishing between different types of interaction patterns with commonly used metrics
requires large samples (Del Giudice 2017b), and many correlational studies in this area (including
single-gene correlational G ×E studies) are seriously underpowered for the task. Exciting devel-
opments on this front include new statistical models that combine multiple genes and multiple
environmental variables into a single interaction test ( Jolicoeur-Martineau et al. 2017) and in-
direct methods that use data from twin studies to infer the shape of the underlying interaction
patterns (South et al. 2017).
Although new statistical tools and improved methodology can be expected to yield substan-
tial benefits, we believe that the most pressing challenges in this area are theoretical in nature
(see Del Giudice 2017a,b). For example, detecting an interaction that matches a diathesis stress
template says little about the underlying developmental process, which may involve maladap-
tive vulnerability to stressors, but also adaptive phenotype–environment matching (Del Giudice
2017a). While differential susceptibility research was initially propelled by novel theoretical mod-
els and ideas, over time, the focus of most researchers has shifted to issues of measurement and
data analysis. As a result, theoretical progress has been slow, and many deeper questions remain
unanswered. For example, it is unclear when selection should favor domain-general plasticity
mechanisms that simultaneously regulate multiple traits, versus domain-specific mechanisms that
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only control a particular phenotype (see Belsky & Pluess 2016). Different models of susceptibility
also make different assumptions about the relationship between plasticity and specialization. In
classic generalist–specialist models (Wilson & Yoshimura 1994; see also Frankenhuis et al. 2016a),
generalists can fit into multiple niches owing to increased plasticity, whereas specialists develop
relatively fixed phenotypes. However, a plausible alternative to this model is that plasticity sup-
ports enhanced specialization (Del Giudice 2017a, Murren et al. 2015); in fact, this scenario may
be more consistent with developmentally focused differential susceptibility models because it as-
sumes that heightened physiological and negative emotional reactivity enables plasticity during an
early sensitive period but may not operate that way later in development (after an orchid child spe-
cializes their phenotype). Other unresolved issues concern the relative strength of various sources
of individual differences (e.g., direct effects of the environment versus G ×E interactions), as well
as the role of shared environmental factors (those that act similarly on siblings in the same family)
versus nonshared factors (unique to each sibling) in the development of plasticity (Del Giudice
2016). Only through sustained theoretical effort will it be possible to address these questions and
use the answers to inform empirical research.
The central question addressed in this review is whether childhood exposures to adversity simply
constrain development, as assumed in dysregulation models, or guide it in an adaptive manner. In
this section, we use the example of pubertal development to demonstrate how both processes oper-
ate simultaneously. Early life stress exposures result in long-term, potentially permanent changes
in physiological systems that both constrain development (increasing morbidity and mortality
risks) and adaptively calibrate it to enhance fitness under stressful conditions. Stress-mediated
development of alternative life history strategies is the key to understanding this dual process.
Biological embedding of early life stress functions to calibrate life history–related traits, including
timing of puberty; allostatic load and associated mental and physical impairments can be under-
stood, in part, as costs and side effects of these adaptive processes.
Timing of Puberty: A Case Study
Pubertal maturation is a dynamic biological process—punctuated by visible changes in stature,
body composition, and secondary sexual characteristics—that culminates in the transition from
the prereproductive to the reproductive phase of the human life cycle (Ellis 2004). Perhaps the
most striking feature of human pubertal and sexual development is its variation. Some individuals
complete puberty in elementary school, while others are still relatively undeveloped when they start
high school; some begin sexual activity and reproduction as teenagers, while others delay having
children until decades later; some pursue short-term sexual relationships with multiple partners,
while others commit to a single long-term partner for life. This variation begins with individual
differences in maturation of the reproductive axis—when and how fast puberty occurs—and then
feeds forward to many other reproductive characteristics.
Early timing of puberty is an important component of a fast life history strategy. Women
who experience early pubertal development, compared with their later-maturing peers, tend to
have higher levels of serum estradiol and lower sex hormone binding globulin concentrations
that persist through 20–30 years of age; have shorter periods of adolescent subfertility (the time
between menarche and attainment of fertile menstrual cycles); experience earlier ages at first
sexual intercourse, first pregnancy, and first childbirth; engage in more risky sexual behavior; and
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as young adults (Belles et al. 2010, Najman et al. 2009; for reviews, see Baams et al. 2015, Ellis
2004, Ibitoye et al. 2017). This covariation between timing of pubertal development and other
life history–related traits supports the conceptualization of puberty as a key switch point in the
development of alternative life history strategies (Ellis 2013).
An Evolutionary–Developmental Theory of Pubertal Variation
Drawing on life history concepts, Belsky et al. (1991) proposed an evolutionary–developmental
theory linking levels of psychosocial stress and support in and around the family to subsequent
timing of puberty and related life history traits. The theory posited that (a)ecologicalcondi-
tions and family dynamics shape children’s early attachment patterns and behavioral development
and, through these developmental processes, subsequent pubertal development and reproductive
strategy, and that (b) this environmentally sensitive developmental system evolved as a means of
matching individuals to their environment in a manner that promotes survival and reproduction
across varying ecological contexts. Over the course of our evolutionary history, individuals growing
up under dangerous or unpredictable family conditions may have reliably increased their repro-
ductive success by accelerating physical maturation and beginning sexual activity and reproduction
at a relatively early age (Belsky 2012, Belsky et al. 1991, Ellis 2004).
When evaluating this theory, a starting assumption is that the effects of physical and psychoso-
cial stressors on pubertal timing are hierarchically ordered: Pubertal timing is contingent firstly
on health and nutrition (see especially Kyweluk et al. 2018) and secondly, when these are ade-
quate, on socioemotional conditions (Coall & Chisholm 2003, Ellis 2004). Consistent with life
history models (e.g., Belsky et al. 1991), a substantial body of literature indicates that, when en-
ergetic conditions are adequate to support growth, early exposures to childhood adversities (e.g.,
socioeconomic adversity, child maltreatment, lack of family warmth and supportiveness, height-
ened parent–child conflict, father absence) tend to predict earlier pubertal development in females
(for reviews, see Belsky & Shalev 2016, Ellis 2004, Webster et al. 2014). For example, in a large
prospective study of a population-based birth cohort in Australia, extremely unfavorable socio-
economic conditions predicted a fourfold increase in boys and twofold increase in girls in rates
of early puberty (Sun et al. 2017a; for convergent findings in a prospective study of a multiethnic
cohort of girls in the United States, see Hiatt et al. 2017). Similar effects may occur in response
to natural disasters. In a large Chinese study, exposure to the Wenchuan earthquake predicted a
fourfold increase among preschool-age girls (under age 7 at the time of exposure) and a twofold
increase among school-age girls (age 7 or older at the time of exposure) in rates of early menarche
(Lian et al. 2018), suggesting an early sensitive period for stress-mediated acceleration of puber-
tal development. Although earlier puberty is associated with childhood exposure to a variety of
psychosocial stressors, the most consistent psychosocial predictor of early puberty in females is
a history of sexual abuse (e.g., Magnus et al. 2018, Mendle et al. 2016). Furthermore, consis-
tent with the assumption that the effects of physical and psychosocial stressors are hierarchically
ordered, childhood deprivation (e.g., food insecurity, neglect) appears to delay pubertal develop-
ment, while childhood exposure to violence (a key marker of extrinsic morbidity and mortality)
appears to accelerate it (Sumner et al. 2018), as per the findings on sexual abuse.
The current evolutionary–developmental model (Belsky et al. 1991) underscores the impor-
tance of conceptualizing pubertal development as part of a developmental continuum, whereby
certain familial and ecological stressors in childhood accelerate pubertal maturation, which in turn
regulates important dimensions of mating and parenting effort. The results of a small number of
prospective, longitudinal studies indicate that the effects of stressful family environments (e.g.,
harsh maternal behavior, paternal unemployment, child maltreatment) on the development of
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faster life history strategies in women (e.g., risky or advanced sexual behavior; intimate partner
violence; and early smoking, drinking, and parenthood) are partially mediated by timing of pu-
berty (Arim et al. 2011, Belsky et al. 2010, Foster et al. 2008, James et al. 2012, Negriff et al.
2015). In sum, puberty appears to operate as an important intervening mechanism linking rearing
conditions to alternative life history strategies.
Accelerated Pubertal Maturation Trades Off Against Health
Although this environmentally sensitive regulation of life history strategies is presumed to be
adaptive, adaptive does not mean cost free. Stress-mediated acceleration of pubertal development
may induce trade-offs that compromise health and curtail the reproductive life span. A history
of sexual abuse is associated not only with earlier age of menarche but also with earlier age
of menopause (Magnus et al. 2018), as well as many other costs to mental and physical health
(e.g., Trickett et al. 2011). Likewise, Bleil and colleagues (2012, 2013) found that psychosocial
stress was associated with earlier puberty and higher antral follicle count in younger women, but
with ovarian reserve depletion in older women. That stress-mediated acceleration of pubertal
development results in wear and tear on the reproductive system converges with a large body of
human research indicating that the development of faster life history strategies comes at the cost of
increasing allostatic load (for a review, see Ellis & Del Giudice 2014). Indeed, both cross-sectional
and longitudinal studies have shown that individuals who pursue faster life history strategies suffer
from more mental health problems, medical ailments (e.g., thyroid disease, high blood pressure
or hypertension, ulcers), and physical health symptoms (e.g., sore throat or cough, dizziness)
(Brumbach et al. 2009, Figueredo et al. 2004, Gibbons et al. 2012, Hill et al. 2016, Mell et al.
2018, Sefcek & Figueredo 2010). In sum, stress-mediated regulation of life history strategies guides
development along specific pathways that can be understood as predictive adaptive responses,
despite substantial costs. Such trade-offs reflect the very nature of development under stress.
Consistent with the notion of trade-offs, early timing of puberty in females is associated with
a broad range of mental and physical health problems, ranging from psychopathology to obesity,
cardiovascular disease, and reproductive cancers (e.g., Day et al. 2015, Ellis 2004, Graber et al.
1997). Earlier sexual maturation has been linked to greater allostatic load (Allsworth et al. 2005);
in that context, the links between early puberty and higher morbidity and mortality concur with
the ALM. An emerging literature has begun to test for the mediating role of pubertal timing in
explaining the well-established links between childhood adversity and later mental and physical
health problems. In this case, again, the results of a small number of prospective, longitudinal
studies suggest that the effects of early adversity (e.g., prenatal stress, childhood trauma, child
maltreatment, maternal depression, negative parenting) on behavioral problems and health (e.g.,
substance use, mental health symptoms, global physical health problems, cardiovascular disease
risk) are partially mediated by early timing of puberty (Belsky et al. 2015b, Bleil et al. 2013, Lei et al.
2018, Mendle et al. 2014, Negriff et al. 2015). In sum, earlier timing of puberty appears to mediate
the effects of early adversity on faster life history strategies, on the one hand, and poor health,
on the other hand. Central to the evolutionary–developmental approach presented in this review
is the proposition that these dual outcomes are interconnected through developmental trade-offs.
Stress Response Systems as Mediating Mechanisms in Stress–Puberty Relations
Stress response systems may play an important role in the developmental relationships among
stress, puberty, and health. As reviewed by Ellis & Del Giudice (2014), stress response systems are
functionally implicated in all components of mating and parenting, beginning with sexual mat-
uration. The autonomic nervous system, HPA axis, and hypothalamic–pituitary–gonadal (HPG) Developmental Adaptation to Stress 129
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axis are connected by extensive functional cross talk (Ellis 2004, Joos et al. 2018). As reviewed
by Joos et al. (2018), the HPA and HPG axes tend to operate independently prior to puberty,
become positively coupled in early adolescence, but then may shift toward negative coupling (or
less positive coupling) in later adolescence (although positive diurnal coupling of cortisol and
testosterone has been observed throughout the life course; Harden et al. 2016). This develop-
mental pattern concurs with a substantial body of research indicating that psychosocial stressors
generally provoke early or accelerated development of the HPG axis in girls but suppressed ovar-
ian functioning in adult women (for a review, see Ellis 2004). For example, in a study of Chinese
elementary school children, greater chronic daily activation of the HPA axis, as indicated by hair
cortisol concentrations (representing chronic stress over the 3 months preceding measurement),
predicted greater testicular volume in boys and breast development in girls aged 6 to 9 years (Sun
et al. 2017b). Likewise, in a longitudinal study in the United States, higher basal cortisol levels at
4 years of age partially mediated the relationship between early adversity exposures and attainment
of adrenarche (the onset of adrenal androgen production) by 7 years of age (Belsky et al. 2015b).
This pattern then apparently switches in later adolescence. In a separate longitudinal study in the
United States, attenuated (rather than elevated) cortisol reactivity to social stress predicted faster
tempo of puberty in adolescent girls (but not boys) aged 9 to 13 years (Saxbe et al. 2015).
In sum, consistent with the notion of positive coupling of the HPA and HPG axes early in
adolescence followed by negative (or less positive) coupling later in adolescence, high pre- and
peri-pubertal basal activation of the HPA axis, but attenuated HPA responsivity during puberty,
was linked to accelerated sexual development—an indicator of a faster life history strategy. Most
interesting, Ruttle et al. (2015) found that stressful family conditions in early childhood accelerated
both the onset of positive HPA–HPG coupling (by age 11) and the transition to negative HPA–
HPG coupling (by age 13) in adolescent girls. Simmons et al. (2015) found that HPA–HPG cou-
pling was positive only in 15–16-year-old girls from low- to moderate-adversity backgrounds, and
that HPA–HPG functioning was uncoupled by that age in girls from high-adversity backgrounds.
Although more research is clearly needed, and the transition toward less positive HPA–HPG cou-
pling may begin quite early in pre-adolescent girls growing up under stressful conditions (Black
et al. 2018), early HPA–HPG coupling could serve as a mechanism through which childhood stress
promotes earlier pubertal development ( Joos et al. 2018, Ruttle et al. 2015). The Wenchuan earth-
quake study (Lian et al. 2018) suggests that the first 5–7 years of life are a sensitive period for the
effects of early life stress on pubertal maturation [as originally proposed by Belsky et al. (1991)]. In
the context of early life stress (presumably during this sensitive period) and the resulting upregu-
lation of basal cortisol, accelerated positive HPA–HPG coupling in early adolescence may operate
as a permissive signal that hastens the onset of puberty. In turn, accelerated negative HPA–HPG
coupling (or reductions in positive coupling) in later adolescence may hasten progression through
puberty (given attenuated HPA functioning in children who have experienced significant early
adversity) (Doom et al. 2014, Trickett et al. 2010; see above discussion of the transition from vig-
ilant to unemotional patterns of stress responsivity in the section titled Beyond Allostatic Load:
Stress Response Systems as a Mechanism of Conditional Adaptation).
Importance of Differential Susceptibility in Regulation of Pubertal Timing
Despite the findings of the literature reviewed above on psychosocial antecedents of pubertal
timing, the effects of childhood stress on puberty tend to be relatively small, are somewhat in-
consistent across studies, and could reflect gene–environment correlations (rGE) operating on a
background of heritable variation in pubertal timing (e.g., Barbaro et al. 2017, Mendle et al. 2006,
Rowe 2000), although initial polygenic analyses have found only limited support for the rGE
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hypothesis (Gaydosh et al. 2018). Theories of differential susceptibility and biological sensitivity
to context suggest that the weak main effects of environmental variables on many developmental
outcomes may reflect the fact that children differ in whether, how, and how much they are affected
by rearing experiences. As articulated by Belsky (2012), the weak main effects of family context
on pubertal timing may overestimate the impact of family environments in some children and
underestimate it in others.
Consistent with this supposition, both physiological variation in autonomic and adrenocorti-
cal reactivity to stress (Ellis et al. 2011b) and genotypic variation in the estrogen receptor-αgene
relationships on timing of puberty in girls. This pattern of differential susceptibility enhances pu-
bertal responses to childhood adversity in some individuals while attenuating it in others. Although
the findings on ESR1 should be considered tentative due to limited sample sizes, they converge
nicely with experimental research on rodents indicating that the accelerating effects of low levels
of maternal licking and grooming (a form of low parental investment) on pubertal maturation in
female offspring are mediated by increased expression of estrogen receptor-αin specific regions
of the hypothalamus (for a review, see Cameron 2011). Finally, some evidence suggests that early
pubertal development itself may operate as a susceptibility factor that amplifies the effects of par-
enting quality on aggression in a for better and for worse manner (Chen & Raine 2018). If so,
susceptibility factors in middle childhood that enhance pubertal responses to early family stress
(e.g., heightened autonomic and adrenocortical reactivity to stress; Ellis et al. 2011b) may set pro-
cesses in motion that further potentiate susceptibility to family relationships in early adolescence.
What is the nature of developmental adaptation to stress? Does childhood adversity adaptively
shape development or simply constrain it? Following the ALM and other dysregulation models,
one can always make a disease-focused argument emphasizing the deleterious effects of adversity
and its biological mediators (e.g., chronic low-grade inflammation, sensitized cortico-amygdala
threat circuitry, abnormal HPA axis functioning). Indeed, the extensive body of research doc-
umenting the negative effects of allostatic load on health is incontrovertible. This is because
development under stressful conditions necessitates trade-offs: One system is diminished so that
another system can be enhanced or preserved. In the scientific literature on stress and development,
however, these countervailing effects have not been equally studied; as a result, we know vastly
more about the detrimental effects of childhood stress than about its benefits in context. The devel-
opmental literature on puberty and life history strategies reveals both sides of the equation. From
an evolutionary perspective, stress-mediated developmental processes do not exclusively cause
impairments and vulnerabilities; they also promote coherent, integrated, functional responses to
childhood adversity. This includes both short-term adjustments (immediate adaptive responses)
and longer-term adaptations (predictive adaptive responses) that regulate development toward
faster life history strategies, which in turn promote survival and reproduction under harsh and
unpredictable conditions. Mental and physical impairments or disease can be partly understood
as costs and side effects of these adaptive processes. At the same time, variation in biological
sensitivity to context attenuates these effects, with some individuals responding strongly to their
rearing conditions, while others are only weakly affected. In sum, natural selection may favor both
developmental adaptations to stress and differential susceptibility to its effects.
The long-term focus of the ACM and other developmental programming models is critical to
understanding stress–health relations because, to a great extent, allostatic load is a by-product of
the chain of resource-allocation decisions that characterize the development of faster life history Developmental Adaptation to Stress 131
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strategies over the life course. In the literature reviewed above, these resource allocation decisions
are mediated through earlier pubertal development and related life history traits (e.g., earlier
onset of sex and reproduction, more risky and aggressive behavior, stress-adapted cognition). In
the ACM, early life stress is biologically embedded in the parameters of stress response systems
and other neuroendocrine processes that guide alternative developmental trajectories. Mapping
out such functional biobehavioral responses to stress is critical for health risk identification and
health promotion because the costs of developmental adaptations to stress (e.g., allostatic load)
and the potential benefits (e.g., adaptive calibration) are inextricably linked—indeed, one cannot
be understood without the other.
The evolutionary–developmental perspective presented in this review affords a big-picture
view of developmental plasticity and individual differences that integrates a wide spectrum of
findings on stress–health relations. From this perspective, dysregulation models—by emphasizing
the pathways leading directly from adversity to dysfunction—miss something fundamental about
development: the coherent, functional biobehavioral changes that occur in response to stress over
time (Ellis & Del Giudice 2014). We need to understand these functional developmental changes
to more fully understand dysfunction. The problem with many traditional interventions is that they
ignore developmental adaptations to stress. This can result in errors of omission (e.g., missing
key intervening variables in stress–health relations) and misidentification of health risk factors
(e.g., mistaking functional brain changes for dysfunction). Treatment and prevention strategies
that ignore developmental adaptations to stress not only miss the opportunity to leverage these
adaptations for good—working with them to enhance positive outcomes—but also risk fighting
against these adaptations in an uphill battle that they are not likely to win (Ellis et al. 2012a, 2017a).
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
We thank Jay Belsky, Lisa Diamond, and Willem Frankenhuis for comments on an earlier draft
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... The way the present-future trade-off is instantiated at the psychological level might partly result from how it is embodied at the biological level (Ellis & Del Giudice, 2019;, notably through the way organisms optimally allocate their limited stock of energy between reproductive goals and maintenance goals (Ellis & Del Giudice, 2019;. ...
... The way the present-future trade-off is instantiated at the psychological level might partly result from how it is embodied at the biological level (Ellis & Del Giudice, 2019;, notably through the way organisms optimally allocate their limited stock of energy between reproductive goals and maintenance goals (Ellis & Del Giudice, 2019;. ...
... The early years of life -from conception to sexual maturity -represent a sensitive period characterized by rapid development, which makes many biological systems vulnerable to environmental stressors. These stress factors, commonly referred to as environmental adversity, interfere with organisms' developmental trajectories and can have a lasting impact on health, reproduction, cognition and behaviour (Ellis & Del Giudice, 2019 Two lines of hypotheses were tested. The first line of hypotheses consists in testing (1) whether the behavioural measures extracted from the three economic games relate to a single hypothesized latent construct and (2) (4) this negative association is mediated by individuals' life-history strategy. ...
Full-text available
Although cooperation is a fundamental and universal aspect of human social relations, it varies considerably from one individual to another. Environmental adversity, which in humans is related to economic deprivation, instability in the family household and extrinsic mortality, appears to determine some of this variability. Although a relationship between adversity and cooperation has been demonstrated in various studies, its precise nature remains undetermined: in adverse environments, cooperation could be increased or decreased, or even not affected. Furthermore, it is unclear through which channel environmental adversity could possibly affect cooperation. Several explanations have been put forward to answer these questions, which we detail in the first chapter of this thesis. In chapters two and three, we present an explanatory model inspired by life-history theory, which states that organisms must make trade-offs in how to allocate their limited metabolic resources to competing biological functions. Until now, the mediating role of these trade-offs in the relationship between adversity and cooperation has not been studied. Using structural equation models, we therefore tested in two separate studies the idea that this relationship is mediated by a prioritized allocation of resources to reproduction, at the expense of somatic maintenance. In the first study, we showed a negative association between adverse environments and cooperation - here measured by self-reported questionnaires - which was mediated by a latent trade-off characterized by more reproductive effort and poorer health status. In the second study where cooperation was measured with economic games, this pattern was simply absent. The ambiguity of these results questions the accuracy of the methods usually used to measure people's prosocial preferences (e.g., social trust). Overall, two main methods are: self-reported questionnaires and economic games. However, the latter are suspected to lack external validity compared to self-reported questionnaires. Why is this the case and what can be done about it? We argue that economic games decisions made in the laboratory are likely to be influenced by the current situation (the current state of the participants), whereas self-reported questionnaires are designed to measure the average behavior of individuals (a trait that is stable over time and contexts). Indeed, it has been shown that decisions made in various economic games show little stability, in contrast to responses to self-reported questionnaires. In a third study presented in chapter four, we want to test the hypothesis that repeated playing of economic games over a longer period of time counteracts the influence of any momentary states. Thus, repeating the economic games over a longer period of time should bring the average responses of participants closer to their average behavior as measured by the self-reported questionnaires. To test this prediction, we aim to conduct a longitudinal study in which 275 respondents will play 10 separate sessions of 16 'Trust games' each, evenly distributed over a 3-week period. A self-reported questionnaire measuring social trust in the first and last session will also be completed. Finally, in the fifth chapter, we discuss the limitations of our research and point to promising approaches that it may inspire.
... A person experiences many changes in their surrounding environment and individual roles. When an individual faces a new environment or role, they tend to face problems adapting to it (Ellis & Del Giudice, 2019). Studies have shown that during periods of adaptation or transition individuals are more likely to have psychological problems (Crede & Niehorster, 2012;Perera & McIlveen, 2014), and the quality of help they receive to solve their psychological problems have a long-term impact on both their physical and mental development (Wood et al., 2018). ...
... Second, based on the Adaptation Calibration Model (ACM) explains pressure (Del Giudice, Ellis, & Shirtcliff, 2011), to some extent, early stress experiences are not always harmful to the individual or cause the disorder of a physiological and psychological function, and can have positive changes to the sensitivity and adaptability of the individual when in a stressful environment (Ellis & Del Giudice, 2019;Ellis, Oldehinkel, & Nederhof, 2017). In this study, individuals with lower psychological Suzhi may have experienced more stressful situations at an early stage, and these experiences reduced their adaptive sensitivity to the environment, that is, in the face of environmental changes, there will be no greater responsibility, and, thus, no difficulty in adaptation. ...
... Perhaps the most popular individual-level theory is that of live fast, die young, developed from the perspective of evolutionary psychology. It proposes that high distress in infancy and early childhood accelerates aging to speed reproduction to beat the odds against it in future environments expected to be harsh and dangerous, leading to the prediction that affected individuals should reach puberty and sexual debut earlier than average (but prenatal effects are only rarely considered) [48]. However, there is accumulating contrary evidence from primates, non-Western human populations, and historical data. ...
... Sentient social organisms appear to have means of comparing group mates with each other and with themselves as a basis for interacting with each other by, e.g., partnering with trusted cooperative individuals or avoiding those known to cheat. Individuals judged by group mates to be subordinate tend to (i) suffer negative social selection (e.g., rejected as social or sexual partners) and (ii) be dominated by others and therefore experience much unpredictability and uncontrollability, known to increase allostatic load [48]. Skulachev [79] raised these very factors as leading to phenoptosis, citing research showing correlations between mortality and psychological factors such as low emotional support and feeling unable to control one's own life. ...
Full-text available
Vladimir Skulachev's coining of the term "phenoptosis" 25 years ago (Skulachev, V. P., Biochemistry (Moscow), 62, 1997) highlighted the theoretical possibility that aging is a programmed process to speed the exit of individuals posing some danger to their social group. While rapid "acute phenoptosis" might occur at any age (e.g., to prevent spread of deadly infections), "slow phenoptosis" is generally considered to occur later in life in the form of chronic age-related disorders. However, recent research indicates that risks for such chronic disorders can be greatly raised by early life adversity, especially during the prenatal stage. Much of this research uses indicators of biological aging, the speeding or slowing of natural physiological deterioration in response to environmental inputs, leading to divergence from chronological age. Studies using biological aging indicators commonly find it is accelerated not only in older individuals with chronic disorders, but also in very young individuals with health problems. This review will explain how accelerated biological aging equates to slow phenoptosis. Its occurrence even in the prenatal stage is theoretically supported by W. D. Hamilton's proposal that offsprings detecting they have dangerous mutations should then automatically speed their demise, in order to improve their inclusive fitness by giving their parents the chance to produce other fitter siblings.
... The lack of significant relationships is also in line with past literature (Lalumiè re et al., 2001) and could be viewed as support for what several authors (Glenn et al., 2011;Pullman et al., 2021;Zara et al., 2021) have argued that psychopathy is not actually maladaptive per se. However, the fact that psychopathy can be recognised as an adaptive strategy in response to early life stress and harsh environments (Ene et al., 2022), that is beneficial in dangerous situations (Ellis and Del Giudice, 2019), does not make it a prosocial adaptation. ...
Purpose This paper aims to present new evidence from the Cambridge Study in Delinquent Development (CSDD) showing the extent to which obstetric (e.g. abnormal birth weight, confinement at birth, severe abnormality of pregnancy, etc.) and early childhood and family factors (illegitimate child, unwanted conception, family overcrowding, etc.) have predictive effects on psychopathic traits measured later in life at age 48 years. Design/methodology/approach Data collected in the CSDD are analysed. This is a prospective longitudinal study of 411 London men from age 8 to age 61 years. Findings The results suggest that none of the obstetric problems were predictive of adult psychopathy. However, some other early childhood factors were significant. Unwanted conception (by the mother) was significantly associated with high psychopathy. The likelihood of being an unwanted child was higher when the mother was younger (19 years or less), and when the child was illegitimate. The poor health of the mother and living in an overcrowded family were also significant in predicting psychopathy in adulthood, as well as both psychopathic personality (F1) and psychopathic behaviour (F2). Originality/value These findings suggest the influence of very early emotional tensions and problematic social background in predicting psychopathic traits in adulthood (at age 48 years). They also emphasise the importance of investigating further the very early roots of psychopathic traits.
... From an evolutionary perspective, we suggest that (natural) SD following stressogenic/traumatic event is critical for enabling organisms to adapt to future conditions. 106 We suggest that at least some of the biological responses following traumatic events result in an increase in vigilance and wakefulness and, therefore, cause SD, which may not represent dysfunction but rather biologically adaptive strategies for dealing with adversity. ...
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Sleep figures in numerous ancient texts, for example, Epic of Gilgamesh, and has been a focus for countless mystical and philosophical texts. Even in the present century, sleep remains one of the most complex behaviors whose function still remains to be further explored. Current hypotheses suggest that among other functions, sleep contributes to memory processes. Memory is a core topic of study in post-traumatic stress disorder (PTSD) and other stress-related phenomena. It is widely accepted that sleep plays a major role in the consolidation of newly encoded hippocampus-dependent memories to pre-existing knowledge networks. Conversely, sleep deprivation disrupts consolidation and impairs memory retrieval. Along this line, sleep deprivation following a potentially traumatic event may interfere with the consolidation of event-related memories and, thereby, may reduce long-term post-traumatic stress-related symptoms. This review consolidates clinical and animal studies on the relationships between sleep, sleep deprivation, memory processes, and trauma exposure while introducing new contemporary insights into an ancient African tribal ritual (Àìsùn Oku) and Japanese ceremony ritual (Tsuya). We propose that these findings, focusing specifically on the effects of sleep deprivation in the immediate aftermath of traumatic events, may be explored as a possible therapeutic measure. Along with a summary of the field questions on whether sleep is performed "to remember" or "to forget" we lay the rationale for using sleep deprivation as a clinical tool. A tool that may partially prevent the long-term persistence of these traumatic events' memory and thereby, at least partly, attenuating the development of PTSD.
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Although early-life adversity can undermine healthy development, an evolutionary-developmental perspective implies that children growing up in harsh environments will develop intact, or even enhanced, skills for solving problems in high‐adversity contexts (i.e., 'hidden talents'). This Element situates the hidden talents model within a larger interdisciplinary framework. Summarizing theory and research on hidden talents, it proposes that stress-adapted skills represent a form of adaptive intelligence enabling individuals to function within the constraints of harsh environments. It discusses potential applications of this perspective to multiple sectors concerned with youth from harsh environments, including education, social services, and juvenile justice, and compares the hidden talents model with contemporary developmental resilience models. The hidden talents approach, it concludes, offers exciting directions for research on childhood adversity, with translational implications for leveraging stress-adapted skills to more effectively tailor education, jobs, and interventions to fit the needs of individuals from a diverse range of life circumstances.
In this exploratory study, we analyzed the contribution of fathering to relational aggression (RA) in middle childhood and the moderating role of children's temperament and gender. Participants (N = 234; 46% girls) were attending public elementary school (mean age = 8.15; SD = 1.23) in middle-class neighborhoods in two Spanish cities. Fathers provided information about their parenting practices using the Parenting Styles and Dimensions Questionnaire, parents gave data on their child's temperament using the Temperament in Middle Childhood Questionnaire and children provided information about their peers' aggressive behavior using the Mini Direct Indirect Aggression Inventory. Fathering dimensions considered were Authoritative Cold, Authoritative Warm, Physical Punishment, and Insecurity; temperament dimensions considered were negative affect (NA), effortful control (EC), activity (AC), and shyness (SH). Gender, fathering, and temperament dimensions additively accounted for a significant proportion of the variance observed in RA. Several significant interactions suggested that the effect of fathering on RA was moderated by temperament and, in some cases, by children's gender. NA increased the potential risk of Authoritative Cold fathering (CF) and, in boys only, of Insecure fathering, while EC potentiated the protective effect of Authoritative-Warm fathering and, in boys only, buffered the risk effect of CF. SH buffered the risk effect of CF and decreased the protective effect of Authoritative Warm fathering on RA. Lastly, AC also buffered the risk effect of CF on RA. Results are discussed in light of the protective or the vulnerability role of temperament and in relation to models that explain sensitivity differences to environmental contexts.
The current study examined whether secure base script knowledge can buffer against higher concurrent externalizing problems and against relative increases in externalizing problems associated with cumulative family stress. We conducted a one-year longitudinal study with two waves between 2017 and 2019 in which 272 Dutch-speaking Western European children from Flanders (47.8% boys, Mage = 10.20,SDage = 0.60) participated. Secure base script knowledge was associated with lower concurrent externalizing problems ( f2 = 0.03). High levels of secure base script knowledge also buffered against relative increases in externalizing problems associated with cumulative family risk ( f2 = 0.02). These findings suggest that secure base script knowledge can mitigate the negative effects of a stressful family environment on externalizing problems.
Objective: Adrenarche, the biological event marked by rising production of dehydroepiandrosterone and its sulfate (DHEAS), may represent a sensitive period in child development, with important implications for adolescence and beyond. Nutritional status, particularly BMI and/or adiposity, has long been hypothesized as a factor in DHEAS production but findings are inconsistent, and few studies have examined this among non-industrialized societies. In addition, cortisol has not been included in these models. We here evaluate effects of height- (HAZ), weight- (WAZ), and BMI- (BMIZ) for-age on DHEAS concentrations among Sidama agropastoralist, Ngandu horticulturalist, and Aka hunter-gatherer children. Methods: Heights and weights were collected from 206 children aged 2-18 years old. HAZ, WAZ, and BMIZ were calculated using CDC standards. DHEAS and cortisol assays were used to determine biomarker concentrations in hair. Generalized linear modeling was used to examine effects of nutritional status on DHEAS concentrations, as well as cortisol, controlling for age, sex, and population. Results: Despite the prevalence of low HAZ and WAZ scores, the majority (77%) of children had BMI z-scores >-2.0 SD. Nutritional status has no significant effect on DHEAS concentrations, controlling for age, sex, and population. Cortisol, however, is a significant predictor of DHEAS concentrations. Conclusions: Our findings do not support a relationship between nutritional status and DHEAS. Instead, results suggest an important role for stress and ecology in DHEAS concentrations across childhood. Specifically, effects of environment via cortisol may be influential to patterning of DHEAS. Future work should investigate local ecological stressors and their relationship to adrenarche.
Suprachiasmatic nucleus (SCN) in mammals functions as the master circadian pacemaker that coordinates temporal organization of physiological processes with the environmental light/dark cycles. But the causative links between SCN and cardiovascular diseases, specifically the reparative responses after myocardial infarction (MI), remain largely unknown. In this study we disrupted mouse SCN function to investigate the role of SCN in cardiac dysfunction post-MI. Bilateral ablation of the SCN (SCNx) was generated in mice by electrical lesion; myocardial infarction was induced via ligation of the mid-left anterior descending artery (LAD); cardiac function was assessed using echocardiography. We showed that SCN ablation significantly alleviated MI-induced cardiac dysfunction and cardiac fibrosis, and promoted angiogenesis. RNA sequencing revealed differentially expressed genes in the heart of SCNx mice from D0 to D3 post-MI, which were functionally associated with the inflammatory response and cytokine-cytokine receptor interaction. Notably, the expression levels of insulin-like growth factor 2 (Igf2) in the heart and serum IGF2 concentration were significantly elevated in SCNx mice on D3 post-MI. Stimulation of murine peritoneal macrophages in vitro with serum isolated from SCNx mice on D3 post-MI accelerated the transition of anti-inflammatory macrophages, while antibody-mediated neutralization of IGF2 receptor blocked the macrophage transition toward the anti-inflammatory phenotype in vitro as well as the corresponding cardioprotective effects observed in SCNx mice post-MI. In addition, disruption of mouse SCN function by exposure to a desynchronizing condition (constant light) caused similar protective effects accompanied by elevated IGF2 expression on D3 post-MI. Finally, mice deficient in the circadian core clock genes (Ckm-cre; Bmal1f/f mice or Per1/2 double knockout) did not lead to increased serum IGF2 concentration and showed no protective roles in post-MI, suggesting that the cardioprotective effect observed in this study was mediated particularly by the SCN itself, but not by self-sustained molecular clock. Together, we demonstrate that inhibition of SCN function promotes Igf2 expression, which leads to macrophage transition and improves cardiac repair post-MI.
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Decades of fetal programming research indicates that we may be able to map the origins of many physical, psychological, and medical variations and morbidities before the birth of the child. While great strides have been made in identifying associations between prenatal insults, such as undernutrition or psychosocial stress, and negative developmental outcomes, far less is known about how adaptive responses to adversity regulate the developing phenotype to match stressful conditions. As the application of epigenetic methods to human behavior has exploded in the last decade, research has begun to shed light on the role of epigenetic mechanisms in explaining how prenatal conditions shape later susceptibilities to mental and physical health problems. In this review, we describe and attempt to integrate two dominant fetal programming models: the cumulative stress model (a disease-focused approach) and the match-mismatch model (an evolutionary-developmental approach). In conjunction with biological sensitivity to context theory, we employ these two models to generate new hypotheses regarding epigenetic mechanisms through which prenatal and postnatal experiences program child stress reactivity and, in turn, promote development of adaptive versus maladaptive phenotypic outcomes. We conclude by outlining priority questions and future directions for the fetal programming field.
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Background The factors influencing pubertal timing have gained much attention due to a secular trend toward earlier pubertal onset in many countries. However, no studies have investigated the association between the Great earthquake and early puberty. We aimed to assess whether the Wenchuan earthquake is associated with early puberty, in both boys and girls. Methods We used data from two circles of a survey on reproductive health in China to explore the impact of the Wenchuan earthquake on early puberty , and a total of 9,785 adolescents (4,830 boys, 49.36%) aged 12–20 years from 29 schools in eight provinces were recruited. Wenchuan earthquake exposure was defined as those Sichuan students who had not experienced oigarche/menarche before May 12, 2008. Early puberty was identified as a reported onset of oigarche/menarche at 11 years or earlier. We tested the association between the Wenchuan earthquake and early puberty in boys and girls. Then, subgroup analysis stratified by the age at earthquake exposure also was performed. Results In total, 8,883 adolescents (4,543 boys, 51.14%) with a mean (SD) age of 15.13 (1.81) were included in the final sample. In general, children exposed to the earthquake had three times greater risk of early puberty (boys, RR [95% CI] = 3.18 [2.21–4.57]; girls: RR [95%CI] =3.16 [2.65–3.78]). Subgroup analysis showed that the adjusted RR was 1.90 [1.19–3.03] for boys and 2.22 [1.75–2.80] for girls. Earthquake exposure predicted almost a fourfold (RR [95%CI] = 3.91 [1.31–11.72]) increased risk of early puberty in preschool girls, whereas the increase was about twofold (RR [95%CI] = 2.09 [1.65–2.64]) in schoolgirls. Among boys, only older age at earthquake exposure was linked to early puberty (RR [95%CI] = 1.93 [1.18–3.16]). Conclusions Wenchuan earthquake exposure increased the risk of early puberty in boys and girls, and preschoolers were more at risk than schoolchildren. The implications are relevant to support policies for those survivors, especially children, to better rebuild after disasters.
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Developmental plasticity is a widespread property of living organisms, but different individuals in the same species can vary greatly in how susceptible they are to environmental influences. In humans, research has sought to link variation in plasticity to physiological traits such as stress reactivity, exposure to prenatal stress-related hormones such as cortisol, and specific genes involved in major neurobiological pathways. However, the de- terminants of individual differences in plasticity are still poorly understood. Here we present the novel hy- pothesis that, in both sexes, higher exposure to androgens during prenatal and early postnatal life should lead to increased plasticity in traits that display greater male variability (i.e., a majority of physical and behavioral traits). First, we review evidence of greater phenotypic variation and higher susceptibility to environmental factors in males; we then consider evolutionary models that explain greater male variability and plasticity as a result of sexual selection. These empirical and theoretical strands converge on the hypothesis that androgens may promote developmental plasticity, at least for traits that show greater male variability. We discuss a number of potential mechanisms that may mediate this effect (including upregulation of neural plasticity), and address the question of whether androgen-induced plasticity is likely to be adaptive or maladaptive. We conclude by offering suggestions for future studies in this area, and considering some research designs that could be used to empirically test our hypothesis.
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Variation in life history (LH) traits along the fast-slow continuum (referred to as pace of life, POL) is thought to result from a trade-off between investments in current versus future reproduction. Originally developed for understanding variation in LH strategies at the among-population level, the POL theory has more recently been applied towards understanding variation in LH traits at the within-population level, and further extended to address the covariance of LH traits with additional behavioural and/or physiological traits, referred to as pace-of-life syndromes (POLS). The article by Réale et al. (Philos T Roy Soc B 365:4051–4063, 2010), which synthesized several earlier reviews and opinions on among-individual covariation between LH, behavioural, and physiological traits, and subsequent research testing POLS in a variety of species, have collectively been cited several hundreds of times—a trend that continues. These works have interdisciplinary impact, informing research in life history biology, behavioural and developmental biology, and the social sciences. In this paper, we review the existing theoretical POLS models that provide adaptive explanations for covariances between LH traits and additional behavioural and/or physiological traits while assuming a trade-off between current and future reproduction. We find that the set of relevant models is small. Moreover, models show that covariances between life history traits and behavioural or physiological traits can arise even in the absence of a current-future reproduction trade-off, implying that observing such covariances does not provide a strong indication regarding the process generating POLS. We discuss lessons learned from existing models of POLS, highlight key gaps in the modelling literature, and provide guidelines for better integration between theory and data.
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Although growing up in an adverse childhood environment tends to impair cognitive functions, evolutionary-developmental theory suggests that this might be only one part of the story. A person’s mind may instead become developmentally specialized and potentially enhanced for solving problems in the types of environments in which the person grew up. In the current research, we tested whether these specialized advantages in cognitive function might be sensitized to emerge in currently uncertain contexts. We refer to this as the sensitized-specialization hypothesis. We conducted experimental tests of this hypothesis in the domain of working memory, examining how growing up in unpredictable versus predictable environments affects different facets of working memory. Although growing up in an unpredictable environment is typically associated with impairments in working memory, we show that this type of environment is positively associated with those aspects of working memory that are useful in rapidly changing environments. Importantly, these effects emerged only when the current context was uncertain. These theoretically derived findings suggest that childhood environments shape, rather than uniformly impair, cognitive functions.
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Currently, two main approaches exist to distinguish differential susceptibility from diathesis-stress and vantage sensitivity in genotype x environment interaction (GxE) research: Regions of significance (RoS) and competitive-confirmatory approaches. Each is limited by their single-gene/single-environment foci given that most phenotypes are the product of multiple interacting genetic and environmental factors. We thus addressed these two concerns in a recently developed R package (LEGIT) for constructing GxE interaction models with latent genetic and environmental scores using alternating optimization. Herein we test, by means of computer simulation, diverse GxE models in the context of both single and multiple genes and environments. Results indicate that the RoS and competitive-confirmatory approaches were highly accurate when the sample size was large, whereas the latter performed better in small samples and for small effect sizes. The confirmatory approach generally had good accuracy (a) when effect size was moderate and N >= 500 and (b) when effect size was large and N >= 250, whereas RoS performed poorly. Computational tools to determine the type of GxE of multiple genes and environments are provided as extensions in our LEGIT R package.
Puberty is often implicated in the onset or exacerbation of psychopathology during adolescence, and pubertal timing and tempo have emerged as important predictors of wellbeing. In the psychosocial literature there is a tendency to view individual differences in the nature (timing and tempo) of pubertal development as either determined by stress experienced in childhood or as a determinant of the development of psychopathology; few studies, however, have examined puberty as both. We propose that pubertal timing and tempo are neither simply antecedents nor consequences with respect to onset or exacerbation of psychopathology, but rather as markers of accumulating risk such as that conceptualized as allostatic load. Further, we propose that integrating coping and self-regulation into models of off-time pubertal maturation presents an opportunity to forge linkages among the processes that precede and follow pubertal development, which may provide malleable intervention targets to offset the costs of early life stress and off-time maturation. The present narrative review synthesizes research from the following literatures: (1) the role of stress in determining the timing and tempo of pubertal development; (2) the role of stress in influencing how pubertal development affects socioemotional and behavioral outcomes during adolescence, and (3) the role of coping and self-regulation in understanding conditional adaptations to stress. Given the conclusions of this synthesis, critical recommendations are made for research and intervention work with adolescents.
Background: Recent conceptual models argue that early life adversity (ELA) accelerates development, which may contribute to poor mental and physical health outcomes. Evidence for accelerated development in youths comes from studies of telomere shortening or advanced pubertal development following circumscribed ELA experiences and neuroimaging studies of circuits involved in emotional processing. It is unclear whether all ELA is associated with accelerated development across global metrics of biological aging or whether this pattern emerges following specific adversity types. Methods: In 247 children and adolescents 8 to 16 years of age with wide variability in ELA exposure, we evaluated the hypothesis that early environments characterized by threat, but not deprivation, would be associated with accelerated development across two global biological aging metrics: DNA methylation (DNAm) age and pubertal stage relative to chronological age. We also examined whether accelerated development explained associations of ELA with depressive symptoms and externalizing problems. Results: Exposure to threat-related ELA (e.g., violence) was associated with accelerated DNAm age and advanced pubertal stage, but exposure to deprivation (e.g., neglect, food insecurity) was not. In models including both ELA types, threat-related ELA was uniquely associated with accelerated DNAm age (β = .18) and advanced pubertal stage (β = .28), whereas deprivation was uniquely associated with delayed pubertal stage (β = -.21). Older DNAm age was related to greater depressive symptoms, and a significant indirect effect of threat exposure on depressive symptoms was observed through DNAm age. Conclusions: Early threat-related experiences are particularly associated with accelerated biological aging in youths, which may be a mechanism linking ELA with depressive symptoms.
Girls who experience father absence in childhood also experience accelerated reproductive development in comparison with peers with present fathers. One hypothesis advanced to explain this empirical pattern is genetic confounding, wherein gene-environment correlation (rGE) causes a spurious relationship between father absence and reproductive timing. We test this hypothesis by constructing polygenic scores for age at menarche and first birth using recently available genome-wide association study results and molecular genetic data on a sample of non-Hispanic white females from the National Longitudinal Study of Adolescent to Adult Health. We find that young women's accelerated menarche polygenic scores are unrelated to their exposure to father absence. In contrast, polygenic scores for earlier age at first birth tend to be higher in young women raised in homes with absent fathers. Nevertheless, father absence and the polygenic scores independently and additively predict reproductive timing. We find no evidence in support of the rGE hypothesis for accelerated menarche and only limited evidence in support of the rGE hypothesis for earlier age at first birth.
Objective: An association between childhood trauma and adult health outcomes has been widely reported, but little is known about the developmental pathways through which childhood trauma influences adult cardiovascular disease (CVD). Methods: Hypotheses were tested with a sample of 405 African Americans from the Family and Community Health Study (FACHS). Path modeling was used to test our theoretical model. Results: Replicating prior research, exposure to childhood trauma was associated positively with increases in symptoms of CVD risk across young adulthood even after controlling for a variety of health-related and health behavior covariates. Further, the association of childhood trauma with CVD risk was mediated by early pubertal maturation. There were no gender differences in the magnitude of this effect. Conclusion: Our findings support an evolutionary-development perspective (Belsky & Shalev, 2016) suggesting that early adverse life experiences lead to early biologically embedded changes reflected in early physical maturation and that these early changes predict later negative adult health outcomes. The results imply that early pubertal maturation is a precursor to vulnerability to long-term health problems. From an intervention standpoint, identifying such developmental pathways may help inform future health-promoting interventions.