Article
Biology, Genes, and Resilience: Toward
a Multidisciplinary Approach
TRAUMA, VIOLENCE, & ABUSE
14(3) 195-208
ª The Author(s) 2013
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DOI: 10.1177/1524838013487807
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Lucy Bowes1 and Sara R. Jaffee2,3
Abstract
Variability in response to stressful environmental exposures is at the core of resilience research. In order to understand why
some individuals show resilient functioning in the face of adversity, one needs to understand the mechanisms through which risky
environments lead to pathology in some and not others, and the ways in which risk and protective factors affect these processes.
Understanding the interplay between genetic and biological processes and different environments is necessary in order to
elucidate the causal pathways through which individuals show resilience or vulnerability in the face of adversity.
Keywords
resilience, biology, genetics, multidisciplinary, maltreatment
There is great variation in the ways in which individuals
respond and react to environmental stressors. While exposure
to risk may lead to psychopathology and ill-health for some,
others show a relative resistance to a similar level of risk, or are
able to overcome the stress or adversity (Rutter, 2006b). It is
assumed that by discovering the mechanisms that underlie this
variation, researchers will shed light on the causal processes for
psychopathology. Given the recent paradigm shift in the importance given to childhood experiences and early environmental
influences for long-term health (Center of the Developing
Child, 2012; Marmot, 2005; Shonkoff & Garner, 2012),
research into the mechanisms through which individuals show
resilience in the face of adversity is gaining momentum. Resilience research is a strengths-based approach that will add to
the knowledge base for policies and programs aiming to promote competence and shift the course of development in more
positive directions for those at risk (Masten & Coatsworth,
1998). The majority of studies on resilience have focused on
psychosocial factors that influence how an individual responds
to stressors, including individual, interpersonal, and family
characteristics together with broader environmental factors
(Curtis & Cicchetti, 2003). More recently, researchers have
argued that a more interdisciplinary approach is needed in
order to uncover the multilevel processes involved in resilient
adaptation to stress (Cicchetti & Rogosch, 2009; Masten &
Obradovic, 2006; Rutter, 2006b). In particular, a better understanding of the role of biological and genetic processes, and
most importantly, how these interact with features of the environment is needed if we are to elucidate the causal processes
involved.
In this review, we begin by giving an overview of what is
meant by the term resilience, and how it may be assessed on
multiple levels, from distal cultural influences down to the
subcellular level. We then consider what is meant by ‘‘stress’’
in the context of resilience, focusing both on psychological
and on biological aspects. We examine how genetically
informed studies of resilient adaptation help elucidate the
causal processes through which distal and proximal environmental stressors influence health and behavior, and why
‘‘one-size-fits-all’’ changes to the environment may not benefit all individuals. We summarize by giving an overview of
how biological and genetic approaches have enriched our
understanding of resilience, and highlight some of the key
questions that remain.
Defining Resilience
Resilience has been defined in multiple ways; however, most
definitions encompass the overcoming of stress or adversity,
or a relative resistance to environmental risk (Garmezy &
Masten, 1994; Masten, 2001; Rutter, 2006c). Rutter emphasizes the interactive component of resilience, namely the combination of serious risk experiences and a relatively positive
psychological outcome despite those experiences (Rutter,
2006c). This is not to say that an individual should only be considered resilient if he or she shows relatively positive outcomes
1
Department of Social Policy and Intervention, University of Oxford, UK
Department of Psychology, University of Pennsylvania, US
3
Social, Genetic, and Developmental Psychiatry Centre, King’s College
London, Institute of Psychiatry, London, UK
2
Corresponding Author:
Lucy Bowes, Department of Social Policy and Intervention, University of
Oxford, Barnett House, 32 Wellington Square, Oxford, OX1 2ER.
Email: lucy.bowes@spi.ox.ac.uk
196
across all domains of functioning. Indeed, it has been argued
that just as we should not expect uniform, consistent positive
development across multiple emotional, behavioral, and cognitive domains in normative development, we should not expect
individuals exposed to stress to show uniform positive outcomes (Luthar, Cicchetti, & Becker, 2000). The outcome
assessed in different studies investigating resilience processes
should be selected according to the specific environmental
stressor being investigated. As will be discussed, there should
be sufficient evidence to believe that the stressor plays a causal
role in the development of the psychopathological outcome
under study. In this review, we highlight biological studies that
may provide useful outcomes for measuring resilience in addition to more standard measures of cognitive, emotional, and
behavioral scores.
The importance of the interactive component used in this
definition of resilience should also be clarified. A statistical
interaction may not always be observed. For a statistical interaction to be observed, there would need to be variation in both
the environmental exposure and the outcome measured. As
highlighted by Rutter (Rutter, 2006c), there are instances in
which no statistical interaction would be observed despite
known individual variation in response to an environmental
stressor, namely when there is a lack of variation in risk exposure. For example, there is much variation in risk of malaria,
with some of the variation explained by genes. However, in
areas endemic for the disease where nearly all individuals are
exposed to a similar degree of risk, no statistical interaction
would be observed, despite the likely biological interaction.
Emphasizing the interactive concept with regard to definitions of resilience helps explain why resilience is not simply
a trait that can be measured directly. As will be discussed later,
different stressors are associated with different phenotypic
outcomes, and it follows that individuals may be resilient to
certain environmental stressors and not others. The same environmental insults to the body also affect individuals in a multitude of ways, and again it follows that people may be
considered resilient for certain outcomes but not others. It is
also necessary to take a life-course approach when investigating resilience processes; people may be resilient at certain
points in their life, but not others. Resilience can be thought
of as a dynamic process (Luthar et al., 2000) rather than an individual trait. From the prenatal period to early childhood and
beyond, human development is understood to be driven by an
ongoing interaction between biology and ecology (Shonkoff
& Garner, 2012). The field of resilience research requires a
better understanding of the role of biological and genetic processes, and most importantly, how these interact with features
of the environment to influence individual variation in response
to stress. Research has long since moved past outdated ideas of
‘‘nature versus nurture’’ (Sameroff, 2010). How an individual
responds to an external stressor will depend on the complex
interplay between a multitude of factors, relating both to
individual characteristics (including genetic factors) and to
the broader environment, including, as noted by Ungar and
colleagues in this issue, the cultural context.
TRAUMA, VIOLENCE, & ABUSE 14(3)
Consider, for example, the case of malaria. Individual characteristics may influence the likelihood of a person contracting
the disease when exposed to infected mosquitoes. One example
in the resilience literature of how genes may be ‘‘protective’’ is
that of sickle-cell disease and risk for malaria. Sickle-cell disease is a recessive genetic blood disorder that causes various
health complications and a decreased life expectancy. Sicklecell disease is more common in tropical and subtropical
areas where malaria is common (Aidoo et al., 2002; Rutter,
2006a), as individuals who carry only a single copy of the
recessive gene that gives rise to sickle-cell disease are at
reduced risk of contracting malaria, and show less severe
symptoms when infected. Thus, having the sickle-cell trait
(i.e., being a single carrier of sickle-cell genes) is a protective
factor in areas with a high rate of malaria. An individual’s likelihood of contracting malaria cannot be calculated simply on
the basis of their genotype however. Clearly there are many
other risk and protective factors that will play a role; how often
is the individual exposed to mosquitoes? Are there regional
policies to eradicate mosquitoes, and is there access to antimalarial treatments? Does the individual wear protective clothing,
insect repellant, or have access to mosquito nets? Similarly, an
individual’s likelihood of resilient functioning following exposure to trauma is unlikely to be attributed solely to either
genetic or environmental factors. It is the complex interplay
between the individual and their environment that will be key
to understanding processes of resilience.
Measuring Resilience
Studies of resilience require accurate measures of environmental
pathogens. The very concept of resilience requires variability
in response to an environmental stressor; not all individuals are
affected by risk exposure in the same way—some appear resilient while others more vulnerable. What is important however
is that the measure of the risk exposure remains the same. It
does not make sense to talk of resilience if one individual was
simply exposed to less risk—either in terms of severity or duration of risk. This is no easy task. Measures of risk exposure are
never perfectly precise or reliable. Furthermore, the very concept of the risk may differ across groups or cultures. For example, what constitutes child maltreatment in one culture, or at
one time in history, may not in another. Physical punishment
is associated with behavioral problems among European Americans but not among African Americans, though physical abuse
predicts behavioral problems equally well across these and
other ethnic groups (Deater-Deckard, Dodge, Bates, & Pettit,
1996). Indeed, physical punishment and strict parenting may
be regarded as evidence of parent’s involved caregiving in
some communities (Chen & Luster, 2002; Mosby, Rawls,
Meehan, Mays, & Pettinari, 1999). Cultural consideration is
therefore needed in studies of resilience following exposure
to particular risk factors. Better measures are also needed for
more distal environmental risk exposures.
Historical, cultural, demographic, and geographic characteristics are important considerations in studies of resilience.
Bowes and Jaffee
Socioeconomic inequalities in risk for ill-health have been the
focus of extensive research (Marmot et al., 1991). At the neighborhood level, disadvantage such as impoverishment, child
care burden, and isolation have been significantly associated
with an increased rate of child maltreatment (Coulton, Korbin,
Su, & Chow, 1995); however, the exact processes that account
for this relationship are not well understood (Coulton, Crampton, Irwin, Spilsbury, & Korbin, 2007). It could be that neighborhood characteristics have a direct effect on parents and
children, for example, through perceived environmental stress
or access to social support, resulting in an increased risk of abusive behavior. The ways in which child abuse is defined, recognized, and reported may also differ between neighborhoods
leading to spurious effects. Neighborhood selection may also
play a role. To the extent that residence in disadvantaged neighborhoods reflects individual characteristics that maintain
downward social mobility, associations between neighborhood
characteristics and risk of child maltreatment may be confounded by parent and family factors.
At the family level, socioeconomic disadvantage has been
repeatedly found to be associated with mental health problems
in children. More focused studies have indicated that the effects
of this relatively distal risk factor are mediated through parent–
child relationships and not lack of money per se (Conger &
Elder, 1994; Costello, Compton, Keeler, & Angold, 2003;
Moffitt, Caspi, & Rutter, 2006). Understanding the mediating
mechanisms through which stressful environments affect individuals is a necessary component in studies of resilience.
Developmental psychopathologists have stressed the need to
adopt an ecological framework to examine the multiple influences on vulnerability and resilience to environmental insults
(Cicchetti & Blender, 2006; Curtis & Cicchetti, 2003; Jaffee
et al., 2007; Luthar et al., 2000; Masten, 2007). Uncovering the
pathways through which environmental stressors operating at
different levels of the ecology influence individual behavior
is the key. One critical area of resilience research is investigating the mechanisms through which external environments trigger biological changes within the body.
Stress and Resilience
Being exposed to severe or chronic stress is associated with
both physical and mental ill-health. Exposure to mild or moderate stress is far less likely to lead to psychopathology, and
may even be beneficial to development (Rutter, 1981). Before
going on to explore the biological mechanisms through which
stress is thought to lead to disease and ill-heath, first it is necessary to consider what is meant by the term stress in the field
of resilience. One important point to make is that stress—both
in measurement and in its experience—is somewhat subjective.
The ways in which individuals perceive and interpret stressors
may vary greatly—in some cases as a function of their previous exposure to adverse events (Chen, Langer, Raphaelson,
& Matthews, 2004; Dodge, 1993). Importantly, what may be
construed as significant levels of stress exposure to a resilience
researcher may not be perceived as such by the individual
197
concerned (Gordon & Song, 1994). In such cases, it may be difficult to determine whether the exposure is in fact ‘‘risky.’’ As
noted by Luthar, Cicchetti, and Becker (2000), concerns about
subjective ratings are not confined to resilience research but are
endemic within the field of psychology. Different informants
may give very different ratings of the same construct; for example, ratings of peer relationships may differ widely depending
on who is providing the report—which child, parent, teacher,
or even an ‘‘objective’’ researcher (Achenbach, McConaughy,
& Howell, 1987; Shakoor et al., 2011). Commonly, there is no
‘‘gold standard,’’ but rather different informants tend to provide
valid perspectives that together may provide a more detailed
measure of the construct. In terms of resilience research, it may
be of particular interest to investigate why some individuals
perceive particular stressors as less stressful than the norm
(O’Connor & Rutter, 1996). It would also be of great interest
to investigate whether different perceptions of the same stressor are associated with different physiological and psychological outcomes.
‘‘Stress’’ is not a simple construct. The same stressor may
affect multiple phenotypic outcomes. For example, exposure
to maltreatment in childhood has been linked to higher incidences of depression (Kaufman, 1991; Widom, DuMont, &
Czaja, 2007), posttraumatic stress (Koenen, Moffitt, Poulton,
Martin, & Caspi, 2007), antisocial behavior (Dodge, Bates, &
Pettit, 1990; Jaffee et al., 2005; Widom, 1989), alcoholism and
other forms of substance abuse (Fergusson, Horwood, & Lynskey, 1996; Lansford, Dodge, Pettit, & Bates, 2010), and indicators of physical ill-health, such as an increase in cardiovascular
risk (Danese et al., 2009, 2010). Exposure to multiple types of
maltreatment may be particularly harmful to child development
(Kim & Cicchetti, 2010). The cumulative impact of multiple
forms of childhood stress has been the subject of a series of
studies based on the Adverse Childhood Experiences (ACE)
Study (Foege, 1998). This study has repeatedly shown a graded
response between exposure to multiple childhood stressors
(e.g., psychological, physical, and sexual child abuse, domestic
violence, parental substance abuse problems, caregivers with
mental health difficulties) and a diverse range of outcomes,
including alcoholism, drug abuse, depression, and suicide
attempt, poor self-rated health, sexually transmitted disease,
physical inactivity, and severe obesity (Dube et al., 2003;
Edwards, Holden, Felitti, & Anda, 2003; Felitti et al., 1998).
When conceptualizing stress for studies of resilience, it is
important that the stressful exposure (a) is expected to lead to
serious, negative outcomes and (b) is believed to play a causal
role in bringing about the health outcome of interest. Neurobiological and genetically informative studies help determine
whether a particular stressor meets these two criteria.
How Stress Can Lead to Disease: The
Biology of Stress Response
Early exposure to stress in both rodents and nonhuman primates has been found to influence vulnerability to illness
through long-lasting changes in stress-related systems, and
198
alterations in brain structures believed to be involved in cognition, mood, and behavior (Levine, 2005; Meaney, 2001; Suomi,
1997). One potential mechanism by which stress may influence
development that has received widespread attention is the
hypothalamic–pituitary–adrenocortical (HPA) axis. The HPA
hormonal response system is present in a range of organisms
and is activated in response to numerous stressors (McEwen
& Stellar, 1993; Miller, Chen, & Zhou, 2007; Weiner, 1992).
Activation of the system occurs when neurons in the paraventricular nucleus of the hypothalamus secrete corticotropinreleasing hormone (CRH). The anterior pituitary gland
responds to the presence of CRH by releasing a pulse of adrenocorticotrophin hormone, which is carried through the peripheral circulation to the adrenal glands, which then synthesize
and release cortisol. Cortisol, the most extensively studied
hormone released during this process, exerts an influence on
multiple systems in the body, including the central nervous
system, the immune system, and the metabolic system (Miller
et al., 2007). Cortisol has been viewed as an important mechanism by which chronic stressors get into the body to bring about
disease.
Animal studies have been useful for investigating casual
mechanisms through which controlled exposure to stress may
bring about physiological change. For example, repeated or
prolonged periods of maternal separation have been associated
with changes in the HPA stress-response system in rodents
(Francis, Caldji, Champagne, Plotsky, & Meaney, 1999; Sanchez, Ladd, & Plotsky, 2001). These changes in the HPA axis
coincide with behavioral changes such as an increase in
anxiety-like behaviors and mild cognitive impairments
(Meaney & Szyf, 2005; Sanchez et al., 2001). More adverse
outcomes have typically been observed with earlier and more
prolonged separation (de Kloet & Oitzl, 2003). By observing
physiological changes in response to environmental stressors,
researchers may gain greater insight into factors that increase
vulnerability to the negative sequelae of environmental stressors. Physiological measures may also aid understanding of
which protective factors may play a causal role in promoting
resilience to stress. For example, in research with rodents,
maternal behavior upon reunion from a period of separation
may help protect pups against negative outcomes (Liu et al.,
1997). Specifically, higher levels of maternal licking and
grooming have been associated with a lower HPA response
to stress in adulthood, and a reduction in the degree of cognitive
impairment (Francis, Champagne, & Meaney, 2000).
There have been numerous human studies linking stressors,
cortisol, and disease. For example, childhood exposure to
victimization and maltreatment has been associated with
alterations in cortisol responses to stressful situations (OuelletMorin, Danese, et al. 2011; Ouellet-Morin, Odgers, et al. 2011),
in addition to changes in immune response and function
(Shirtcliff, Coe, & Pollak, 2009), and increases in inflammation levels (Danese et al., 2009). In an innovative study by
Ouellet-Morin and colleagues (2011b), it was noted that children victimized by both adults and peers showed a blunted
cortisol response to a laboratory stress paradigm, in contrast
TRAUMA, VIOLENCE, & ABUSE 14(3)
to nonvictimized children who displayed a normative cortisol
response. Importantly, blunted cortisol response was associated with increased levels of social and behavioral difficulties, but only among victimized children. The findings
indicate that blunted HPA axis reactivity may be an indicator
of increased developmental risk among children exposed to
victimization. It is not known whether these putative effects
on HPA axis reactivity differ in those who overcame the
experience of victimization and displayed resilient functioning. The literature on HPA axis reactivity is highly complex.
For example, in a study by MacMillan and colleagues, a similar attenuated cortisol response to a social stress task was
observed among maltreated female youths but not among a
non-maltreated control group (MacMillan et al., 2009). However, in the MacMillan study, the blunted cortisol reactivity
was not associated with current symptoms of major depressive disorder or posttraumatic stress disorder, perhaps indicating that HPA axis hyporeactivity is more strongly
associated with behavioral difficulties than with emotional
disorders. A recent meta-analysis by Miller and colleagues
(2007) highlights the complex nature of the stress-response
system. It appears that chronic stress has the capacity to
increase or decrease HPA activity, with the resulting pattern
of activity dependent on features of the stress itself and the
individual exposed. The timing and nature of the stressor
appears to impact on findings, as does the controllability and
individual psychiatric response (Dickerson & Kemeny, 2004;
Fries, Hesse, Hellhammer, & Hellhammer, 2005; Miller
et al., 2007; Sapolsky, 1996). Despite these findings, uncertainty remains as to whether changes in the HPA axis do
in fact mediate the effects of environmental stressors on psychological outcomes. Furthermore, evidence is lacking in
whether or not there are differential effects on the HPA system among those who display resilient functioning in the
face of adversity. The findings do, however, suggest important features of both exposures and outcomes that may be
important to consider in studies of resilience, including the
nature and timing of the stressor, the degree to which it may
be ‘‘controllable’’ and the psychiatric outcome in question.
Exposure to Mild Stress: Stress Inoculation
and ‘‘Steeling’’ Effects
Exposure to stress does not always result in damaging physiological or neurological deficits however. Evidence from animal
studies indicates that exposure to lower levels of stress may
result in adaptive biological changes, known in the literature
as ‘‘stress innoculation.’’ For example, squirrel monkeys exposed to repeated, relatively short (i.e., 1- to 6-hr separations)
maternal separations show temporary species-typical signs of
distress (locomotor agitation, distress peep calls, and acute elevations in plasma cortisol levels). After each maternal reunion,
measures return to baseline (Coe, Glass, Wiener, & Levine,
1983; Stanton & Levine, 1985). The outcome of these repeated
separations is that these ‘‘stress-innoculated’’ monkeys show
diminished HPA axis activation in response to subsequent
Bowes and Jaffee
acute stressors and are better able to regulate negative emotional arousal in response to later, acute stressors (Parker &
Maestripieri, 2011). Upon being placed in a novel environment,
stress-inoculated monkeys appear less anxious; they are more
likely to explore novel objects, display decreased clinging to
their mothers, and are better able to use their mothers as a
secure base from which to explore relative to noninoculated
monkeys. Such adaptive responses appear to be associated with
the degree of behavioral control an animal has when confronted
with stress; early experiments with rodents showed that prior
experience of controllable shock blocks the typical behavioral
responses to subsequent uncontrollable shock (Maier, Amat,
Baratta, Paul, & Watkins, 2006; Williams & Maier, 1977).
Whether such effects persist across the life course remains to
be tested (Parker & Maestripieri, 2011). The extent to which
an environmental risk is ‘‘controllable’’ is suggested as a key
aspect of what makes a situation stressful (Heim, Ehlert, &
Hellhammer, 2000; Sapolsky, 1998).
The concept of ‘‘stress inoculation’’ in the animal literature
closely parallels what has been referred to in human studies of
resilience as steeling effects (Rutter, 1981). Very few human
studies have looked at potentially beneficial physiological
changes following exposure to mild or controlled levels of
stress, but behavioral findings indicate that such differences
may be expected. In longitudinal studies investigating children
in California who lived through the great economic depression
of the 1920s and 1930s, it was found that while the social and
behavioral development of younger children tended to be
impaired, older children were sometimes strengthened by the
experience. Elder and colleagues interpreted this finding as
showing that older children who were better able to cope successfully with the increased social and economic responsibilities learned from and were strengthened by the experience
(Elder, 1974). The study of how individuals cope with a stressful encounter at the cognitive and behavioral level has been
the subject of a great deal of research (e.g., Folkman, Lazarus,
Dunkel-Schetter, DeLongis, & Gruen, 1986; Lazarus & Folkman, 1984; Skinner, Edge, Altman, & Sherwood, 2003). Key
factors that help determine whether an experience is associated
with severe symptoms or recovery include appraisal of the situation and considering what is potentially at stake, and the
choice of coping strategies individuals use in order to either
change the stressful situation or modify their emotional
response (Lazarus, 1996). At the physiological level, there is
evidence to suggest that individual differences in coping strategies are associated with differences in neuroendocrine response
to both acute and chronic stress (Olff, 1999). The ways in
which individuals cope with stress clearly plays an essential
role in the process of resilient adaptation.
Constraints to Resilience: Damaged Beyond Repair?
Although successful coping with mild or even moderate stressor may be associated with beneficial outcomes, in cases of
exposure to extreme stress there may be constraints on resilient
adaptation. For example, in a famous study of children adopted
199
from profoundly depriving institutions in Romania, it was
found that children adopted prior to the age of 6 months
showed no persisting deficits, whereas children who spent longer than 6 months in the institutions showed persistent adverse
sequelae even up to age 15, despite many years living with
well-functioning families in the United Kingdom. No increase
in risk was observed beyond the 6-month period, suggesting
that long-lasting physiological or neurological damage may
have occurred by this time (Kreppner et al., 2007). In two
recent follow-up studies, it was shown that individuals who had
spent more than 6 months in the Romanian institutions showed
differences in their brain structure (notably in the amygdala)
and in their brain reward systems compared to a noninstitutionalized comparison group (Mehta et al., 2009, 2010). It remains
to be tested whether the same structural and functional differences may be observed between adopted individuals who spent
less than 6 months versus more than 6 months in the institutions. Thus, there is some indication that there may be a limit
to the possibility of resilient functioning following exposure
to stressful or traumatic experiences. Such studies suggest there
may be ‘‘windows of opportunity’’ for offsetting the pathological consequences of risk exposure, and emphasize the need to
consider timing of risk in studies of resilience. It remains the
case that some exposures may be so damaging to an individual
that the chances of a resilient outcome are slim.
Establishing Causality: How Genetically Informed
Studies Inform Resilience Research
Exposure to stressful experiences has been shown to impact on
biological development in ways that may often confer longterm risk. However, the relationship between exposure to environmental stress and individual development is bidirectional.
Just as certain environments can result in long-term biological
changes, an individual’s biological and genetic makeup can
also alter the types of environment that are experienced, and the
ways in which these experiences are processed. To a certain
extent, individuals self-select themselves into different environments; those who are shy and introverted by nature are likely
to seek out different social experiences than those who are
more extroverted, for example. Genetically influenced behaviors or characteristics may also influence the reaction of others. For example, children who show more withdrawn,
depressive-type behaviors are more likely to be targeted by bullies (Arseneault et al., 2008). Such internalizing behaviors have
been shown to be at least partly heritable (Bartels et al., 2004;
Haberstick, Schmitz, Young, & Hewitt, 2005; Happonen et al.,
2002), and thus it is perhaps not surprising that exposure to peer
victimization has been found to be partially influenced by
genetic factors (Ball et al., 2008; Bowes et al., 2013). The
impact of the family ‘‘environment’’ on children’s development may also be confounded by genetic factors. For example,
experience of maltreatment has long been shown to be associated with conduct problems in children (Dodge et al., 1990;
Lansford et al., 2002; Widom, 1989); however, parents who
maltreat their children are more likely to have a history of
200
antisocial behavior, which in itself is moderately heritable
(Rhee & Waldman, 2002). Thus, it has been argued that maltreatment may be a marker for genetic risk that parents transmit
to children rather than a causal risk factor for children’s conduct problems (DiLalla & Gottesman, 1991; Jaffee & Price,
2007). If the influence of a particular exposure on a behavioral
outcome is genetically mediated, interventions may be better
targeted at changing children’s behavior rather than the risk
exposure itself. In the case of both childhood maltreatment and
peer victimization, research using pairs of genetically identical
twins has indicated that the risk is environmentally mediated
and not simply confounded by shared genetic factors. In
instances where only one twin in a pair has been exposed to victimization, there is a higher rate of psychopathology in the
exposed twin, despite both twins having the same levels of
genetic risk (Arseneault et al., 2008). Thus, targeting exposure
to victimization can be expected to reduce children’s likelihood
of developing emotional and behavioral problems. Such examples highlight why it is important to determine in studies of
resilience that the exposure variable is in fact ‘‘risky,’’ with the
risk being environmentally, rather than genetically, mediated
(Rutter, 2006c).
Gene–Environment Interactions
One of the key reasons why genetically informative research
will enrich the field of resilience is that such studies help elucidate the causal processes that underlie individual variability
in response to stress. It is assumed that knowledge about the
causal mechanisms of stress vulnerability can help guide intervention efforts and help promote resilience in the face of adversity. As described above, genetically informative research can
be used to test for environmental mediation, a prerequisite for
causal pathways between risk exposure and outcome. Genetically informative research is also used to examine the individual variability in response to stress that is at the core of
resilience research, in particular through the study of gene–
environment (G E) interactions. A gene–environment interaction or ‘‘GE’’ is said to occur when the effect of exposure to
an environmental risk factor on health and behavior is moderated by variation in specific genes (or conversely, when the
effect of specific genes is moderated by the environment;
Moffitt, Caspi, & Rutter, 2005). When similarly exposed to a
specific environmental risk, individuals who carry the ‘‘protective’’ version (or allele) of the gene have been reported to show
a reduced risk of susceptibility to psychopathology compared
to individuals with the ‘‘vulnerable’’ allele (Kim-Cohen &
Gold, 2009; Kim-Cohen & Turkewitz, 2012). Importantly, the
genes in themselves do not operate as a risk or protective factors and appear to have little or no effect in the absence of the
environmental risk (Rutter, 2006b).
The first reported finding of a candidate G E influencing
risk for psychopathology in humans came from a study by
Caspi and colleagues in 2002. It had long been known that boys
who experienced maltreatment were at increased risk of antisocial behavior in childhood and adolescence (Widom, 1989),
TRAUMA, VIOLENCE, & ABUSE 14(3)
with some indication that the earlier they were exposed to maltreatment, the greater the risk of behavioral problems (Keiley,
Howe, Dodge, Bates, & Pettit, 2001). It was also noted that
there was a great deal of individual variation in how children
were affected by the experience and that most children did not
go on to become delinquents or criminals (Widom, 1997).
Caspi and colleagues proposed that at least some of this variability in response may be due to genetic ‘‘susceptibility factors’’ that moderate the influence of maltreatment on the
developing child. In particular, deficiencies in the monoamine
oxidase A (MAOA) gene had been reported to be associated
with aggression in rodent studies, with one human case study
of a Dutch kindred finding a similar association with aggression among males with a rare null allele at the MAOA locus
(Brunner, Nelen, Breakefield, Ropers, & van Oost, 1993).
Findings were mixed as to whether MAOA was associated with
aggression in the general population however, although childhood maltreatment was known to correlate with lasting neurochemical changes in neurotransmitter systems affected by
MAOA activity. Caspi and colleagues therefore tested the
hypothesis that MAOA genotype moderates the influence of
childhood maltreatment on neural systems implicated in antisocial behavior by testing for an interaction between MAOA genotype and maltreatment using a longitudinal study design.
Maltreated boys whose genotype conferred relatively low levels of MAOA expression were found to have significantly
higher levels of antisocial behavior in adolescence and adulthood compared to maltreated children who had the highactivity version of the MAOA gene. Importantly, there was
no difference in MAOA genotype between maltreated and nonmaltreated groups, suggesting that MAOA genotype did not
influence exposure to maltreatment. A year later, Caspi and
colleagues reported a second G E, this time involving variants of the serotonin transporter (5-HTT) gene (Caspi et al.,
2003). When exposed to four or more stressful life events, individuals with one or two copies of the 5-HTT ‘‘short’’ allele
were found to have more symptoms of depression, increased
incidence of clinical depression, and increased suicidality compared to individuals with two copies of the ‘‘long’’ allele. A
similar interaction with the 5-HTT gene was observed with
exposure to childhood maltreatment. In both studies, there was
little or no direct main effect of the genotype on the outcome
under investigation, and a relatively small main effect of the
environmental hazard. The largest effect was observed with the
interaction between the ‘‘susceptibility gene’’ and the hazard
(Rutter, 2006a). The genes therefore appear to influence vulnerability to environmental stressors and cannot be thought
of as risk or protective factors in themselves—this is clearly not
a case of ‘‘good’’ genes and ‘‘bad’’ genes.
G E interactions have been the subject of a great deal of
controversy of late. It has been suggested that the many positive replications in the literature have been biased by the existence of publication bias, low statistical power, and a high false
discovery rate—particularly among novel G E studies and
indirect replications, including studies that fail to report
whether they are testing for an additive or multiplicative
Bowes and Jaffee
interaction (Duncan & Keller, 2011). There have been several
meta-analyses examining G E with the polymorphism in the
serotonin transporter gene; however, differences in inclusion
and exclusion criteria have resulted in divergent findings
(Brown & Harris, 2008; Munafo, Durrant, Lewis, & Flint,
2009; Munafo & Flint, 2009; Risch et al., 2009; Uher &
McGuffin, 2008). The heterogeneity in the methods used to
detect G E interactions has impacted the ability of researchers to make an assessment of the overall effect. Specifying features of the environmental pathogen that interact with genes to
predict vulnerability and resilience may be important (KimCohen & Gold, 2009). For example, Brown and Harris
(2008) noted that studies that have failed to replicate the G E
between 5-HTT and life events have measured the occurrence of stressful life events in the months immediately preceding the depressive outcomes (Brown & Harris, 2008). In
contrast, most of the positive replications have been in keeping with the original study by Caspi and colleagues in measuring life events in the 5 years previous to the outcome. If
replicated, this finding could have important implications for
understanding timing effects for how stress ‘‘gets under the
skin’’ to predict depression or resilience. It is also possible
that this observation may be the result of composite measures
of life events being more psychometrically reliable. The
observation highlights the need for resilience studies to use
a longitudinal approach; individuals may appear resilient at
one time point, but may develop problems later on (Jaffee
& Gallop, 2007; Luthar et al., 2000; Rutter, 2006b).
Differential Susceptibility to the Environment
One recent theory that is of relevance to resilience research and
the need to include genetic measures is differential susceptibility to the environment. This theory posits that certain individuals may be more affected by their environment—both for
better and for worse—as a result of their genes (Belsky,
Bakermans-Kranenburg, & van IJzendoorn, 2007; Boyce &
Ellis, 2005). While G E findings have indicated that certain
individuals may be especially vulnerable to the effects of early
stressors according to their genotype, there is also evidence that
under positive rearing conditions, these same children fare better
than children with the ‘‘protective’’ allele (BakermansKranenburg, Van, Pijlman, Mesman, & Juffer, 2008; Pluess,
Belsky, Way, & Taylor, 2010). Thus, rather than thinking of
certain genotypes as conferring vulnerability in the context of
environmental stressors, it may be better to think of these genotypes as conferring plasticity, rendering some individuals
more susceptible than others to both negative and positive environmental influences (Belsky & Pluess, 2009). The theory has
important implications for intervention efforts; children who
are at the greatest risk of developing behavioral problems may
prove to benefit most from prevention and intervention efforts
(Kim-Cohen & Turkewitz, 2012). Emerging experimental evidence provide support for this interesting hypothesis. Compared to children at moderate risk only, children at high risk
of developing conduct problems were more likely to benefit
201
from a multicomponent intervention program targeting key risk
factors (Conduct Problems Prevention Research Group, 2011).
Such findings suggest that the ‘‘life-course persistence’’ of conduct disorders may in fact be malleable, given suitable multifaced intervention efforts. The same genetic variants that
increase risk of psychopathology in adverse circumstances
appear to make individuals more likely to benefit from positive
environmental factors such as social support (Kaufman et al.,
2006; Wilhelm et al., 2006). These studies suggest that, once
identified, targeting those at highest risk may be the most effective (and cost-effective) strategy for prevention and intervention efforts. On the other hand, these findings provide
tentative evidence to suggest that targeting those at low-tomoderate risk may in some cases be less effective or even ineffective. Thus, it may be that ‘‘one-size-fits-all’’ changes to the
environment may not benefit everyone.
The Dynamic Genome: Epigenetics and
Resilience
G E interactions are one example of how genetic factors may
influence resilient responses to stressors. Static differences in
DNA sequence may not be the only way in which genes influence individual differences in response to stress. Although the
string of nucleotides that comprise DNA remain stable
throughout life, the patterns of gene expression and regulation
that result from the DNA is highly dynamic. The ‘‘epigenome’’
provides a further layer of genetic information to the DNA
code. The epigenome regulates genomic functions such as
when and where genes are turned on or off. The term epigenetics is defined in the research literature as the reversible regulation of gene expression, mediated primarily through
changes in DNA methylation and chromatin structure (Jaenisch
& Bird, 2003). Perhaps, the key part of this definition for resilience research is that epigenetics refers to reversible changes
in gene expression. Although DNA sequences and the genes for
which they encode are fixed, the actual expression of genes in
the body is not. There is increasing evidence that epigenetic
processes may be induced following exposure to different environmental insults. For example, changes in diet, hormonal
exposures, or experience of maltreatment have all been shown
to influence patterns of DNA methylation (Zhang & Meaney,
2010), leading to changes in gene expression. These epigenetic
changes are transmitted during mitosis, the normal process of
cell duplication in nonsex cells that occurs throughout the life
course, and thus may provide a mechanism by which certain
environments have long-lasting influences on an individual
(Mill, 2011). Among adults with and without a history of maltreatment, methylation differences have been observed in glucocorticoid genes (McGowan et al., 2009; Zhang, Labonte,
Wen, Turecki, & Meaney, 2012) and in the serotonin transporter
gene (SLC6A4; Beach, Brody, Todorov, Gunter, & Philibert,
2010). In the latter sample, SLC6A4 methylation levels
accounted for the association between a childhood history of
sexual abuse and adult antisocial personality disorder in
women (Beach, Brody, Todorov, Gunter, & Philibert, 2011).
202
Epigenetic mechanisms may help elucidate pathways from risk
to resilience as we begin to understand how environmental
stressors affect the body at the level of the genome. The epigenetic modifications brought about by adverse childhood experiences may modify the expression of functionally relevant genes
involved in the HPA axis (Heim, Newport, Miller, & Nemeroff,
2000; Weaver et al., 2004), immune system (Danese, Pariante,
Caspi, Taylor, & Poulton, 2007), and serotonin transporter
gene (Beach et al., 2010), influencing future stress responses
and vulnerability to depression (Uher, 2008). The dynamic
nature of epigenetic processes demonstrates that genetic influences on behavior are not fixed or unchangeable, but rather are
responsive to the surrounding environment. Environmental
protective factors may serve to alter gene expression and help
set in motion a cascade of positive adaptation to stress. For
example, regular aerobic exercise appears to reduce risk of
anxiety and depression, in addition to improving cognition and
brain function (Rimer et al., 2012 ; Smith et al., 2010). There is
evidence that regular exercise may induce the expression of
genes associated with neuroplasticity and neurogenesis in the
hippocampal region (Collins et al., 2009), as well as helping
to regulate HPA axis response to stress. This suggests that the
beneficial effects of physical exercise might be at least in part a
consequence of epigenetic mechanisms (Dudley, Li, Kobor,
Kippin, & Bredy, 2011). Environmentally driven changes in
gene expression may provide a mechanism through which the
impact of earlier risk exposure can be altered and resilience
promoted. The field of epigenetics research is in its infancy
however, and caution must be used in interpreting findings.
In addition to being highly dynamic, epigenetic profiles are
largely tissue-specific, and it is not clear whether methylation
profiles identified in peripheral tissues (commonly sampled
in human epigenetic studies) will be identified in brain tissue
(Heijeman & Mill, 2012).
Genetically Informative Research and Clinical Utility
One important argument by resilience researchers against the
use of genetic measures in studies of resilience is that there
is little clinical utility; researchers have argued that as genes are
not malleable to change, they offer little help in the development of prevention and interventions aiming to promote resilience among at-risk individuals. The potential impact of G E
interactions on an individual’s vulnerability or resilience to an
environmental stressor is clearly an area warranting further
research; however, such findings are not deterministic; simply
because an individual with a particular genotype is exposed to a
particular environment does not mean that psychopathology is
inevitable. Rather, such individuals may be at increased risk
and could be important candidates for intervention efforts.
Thus, G E research attempts to tackle the question as to who
is at most—and least—risk from an environmental pathogen,
rather than simply the average effect of the risk across all
exposed individuals (Moffitt et al., 2006). G E findings may
also help elucidate how certain environmental pathogens ‘‘get
under the skin’’ to influence vulnerability to psychopathology.
TRAUMA, VIOLENCE, & ABUSE 14(3)
It has been argued that evidence of a specific functional gene
interacting with an environmental stressor brings us closer to
determining the underlying causal pathways of risk and resilience (Moffitt et al., 2006). At present, G E interactions remain
statistical in nature; uncovering the molecular mechanisms by
which G E interactions operate is of crucial importance if the
knowledge is to aid intervention efforts (Mill, 2011).
Even where G E interactions are identified, negative sequelae associated with early stress and genetic vulnerability are not
inevitable. Pyschosocial factors can promote resilience in children exposed to stressful experiences even in the context of
genotypes expected to predispose children to negative outcomes (Kaufman et al., 2006). Recent research indicates that
access to adequate social support promotes emotional resilience in ‘‘genetically vulnerable’’ children with a documented
history of parental abuse (Kaufman et al., 2004, 2006). Specifically, maltreated children with the short allele of the serotonin
transporter gene who received adequate social support were
found to have depression scores that were similar to those of
non-maltreated children. Protective factors may also have differential effects for children exposed to the same stressors but
who have different genotypes in specific, measured genes. Protective factors relating to self-coping styles have been identified that promote emotional resilience in maltreated
adolescents with a ‘‘low-risk’’ genotype (in this instance, high
MAOA activity) but not for ‘‘genetically vulnerable’’ adolescents with low MAOA activity (Cicchetti, Rogosch, &
Sturge-Apple, 2007). The effects of family interventions targeting adverse parenting and disadvantage have been shown to
have genotype-dependent preventative effects on children’s
behavioral problems (Bakermans-Kranenburg & van Ijzendoorn, 2006; Bakermans-Kranenburg et al., 2008). Furthermore, responsivity to psychological treatment for anxiety has
been shown to be greater among carriers of the 5HTTLPR
SS genotype compared to those with the SL/LL genotype in
children with anxiety disorders (Eley et al., 2012). Thus,
genetic research may help elucidate why ‘‘one-size-fits-all’’
changes to the environment may not benefit all individuals.
Through the consideration of biological mechanisms in prevention science, it is hoped that program efficiency will be
increased (Beauchaine, Neuhaus, Brenner, & Gatzke-Kopp,
2008). Biological indicators of risk have already been used to
identify those most in need of prevention and intervention
efforts for certain disorders, helping to direct limited resources
to where they are most needed. Knowledge of underlying biological vulnerability and the ways in which it may moderate
treatment response will also help ensure a better match between
individuals and treatments (Beauchaine et al., 2008; Uher,
2008). Neurobiological studies have also indicated that there
may be physical constraints on resilience, and suggest windows
of opportunity for treatment.
The Biology of Resilience: Future Directions
This review highlights key areas in which knowledge of genetic
predisposition and biological processes will aid studies of
Bowes and Jaffee
resilience. New technologies such as microarrays, genomewide sequencing, and genome-wide associations studies are
expanding our knowledge of the human genome. We are still
a long way from understanding the complex person–environment interactions that underscore resilient adaptation to stress,
however. If it were the case that researchers need only to discover ‘‘protective’’ or ‘‘vulnerability’’ genes that moderate the
impact of specific environmental exposures, one would expect
that rates of psychopathology would be higher in carriers of the
latter genes, given the high rates of environmental exposures
such as maltreatment or life events (Uher, 2011). This is not the
case, suggesting that such a simplistic view of genes is misguided. It is clear that there are multiple sources of vulnerability to disease that unfold over time. The process involves a
complex interplay between biological and psychological vulnerabilities and environmental risk. It will take time and
cross-disciplinary effort to uncover mechanisms of resilience
and vulnerability to disease. Key questions that remain largely
unanswered in the field of resilience research are how biological factors may be protective against stress and how such factors may be harnessed in intervention research. While there is a
large body of research focusing on the mechanisms by which
risky environments ‘‘get under the skin’’ to increase vulnerability to psychopathology, very little is known about the mechanisms by which positive, socially supportive environments ‘‘get
under the skin’’ to promote resilience. The few studies that
have started to address this important question suggest that
there may be genotype-dependent protective effects of psychological and pharmacological interventions (BakermansKranenburg & van Ijzendoorn, 2006; Bakermans-Kranenburg
et al., 2008; Cicchetti et al., 2007; Huezo-Diaz et al., 2009; Serretti, Kato, De Ronchi, & Kinoshita, 2007), although the biological mechanisms themselves remain unclear. Overall, these
early findings lend support to the suggestion that ‘‘one-sizefits-all’’ prevention and intervention efforts are unlikely to benefit all individuals.
Summary
Development occurs through a complex interplay between
genetic predisposition and environmental exposures, and
genetically informed research designs are needed to uncover
the processes that lead to resilience. Genetically informative
studies can be used to test for environmental mediation of measured stressors, bringing us closer to identifying stressors that
have a causal role in the development of psychopathology.
An understanding of genetic predisposition will also give
insight into which individuals may be particularly at risk from
specific stressors, and may facilitate a better understanding of
which children will respond to which types of intervention
(Beauchaine et al., 2008), thus increasing efficiency for intervention programs. Understanding the genetic and biological
mechanisms that underlie individual variation in response to
stress may help elucidate why ‘‘one-size-fits-all’’ changes to
the environment may not benefit all individuals. Knowledge
of epigenetic changes resulting from previous stress exposure
203
may also help identify at-risk individuals and may provide evidence as to which protective factors may reverse changes in
gene expression that have occurred as a response to stress.
Resilient adaptation to environmental insults arises from complex person–environment interactions that can and should be
explored on multiple levels, from distal cultural influences
down to the subcellular level. Understanding the causal processes through which distal and proximal environmental influences affect health and behavior is crucial to the study of
resilience.
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to
the research, authorship, and/or publication of this article.
Funding
The authors disclosed receipt of the following financial support for the
research, authorship, and/or publication of this article: Lucy Bowes is
supported by the Jacobs Foundation. Sara Jaffee is supported by the
Economic and Social Research Council (Grant no. ES/G020132/1)
and by the William. T. Grant Foundation (Grant no. 10909).
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Author Biographies
Lucy Bowes is a Postdoctoral Research Fellow at the Department of
Social Policy and Intervention, University of Oxford. Her research
focuses on the genetic and environmental influences on resilience to
early life stress, with a particular focus on the role of peer
victimization.
Sara R. Jaffee is Associate Professor of Developmental Psychology
at the University of Pennsylvania and Reader in Gene-Environment
Interplay at King’s College London. She is interested in how stressful
environments exacerbate underlying genetic vulnerabilities to affect
children’s development, with a special interest in children’s antisocial
behavior.