Cultural Epigenetics: Biology and Social Systems

Cultural epigenetics
Eva Jablonka
Abstract: Taking a Waddingtonian system approach, I discuss some of the implications
of recent epigenetic research for the study of social systems. A growing number of investigations show that life-style changes resulting from nutritional, toxicological, and
psychological stresses are reflected in changes in the epigenetic profile of individuals,
and that learning and memory have epigenetic correlates. Moreover, various types of
epigenetic changes can be inherited and affect the characters of descendants. Studying
epigenetics can forge new experimental and conceptual bridges between biology, the
social sciences and the humanities. For example, new techniques that allow the deciphering of methylation patterns in ancient DNA could be used to study the epigenetics
of human cultures in long-gone historical periods, thus enriching and extending our
knowledge of human history. Conceptually, an epigenetic perspective blurs traditional
distinctions such as those between nature and nurture, plasticity and evolvability.
Keywords: epigenetics, culture, history, methylation, microbiome, social landscape,
Waddington
Stability and change, canalization and plasticity in social-cultural systems
We observe and experience many changes in our social systems, but change does
not seem to be limitless and random. History is not just ‘one damn thing after
another’: although many changes are surprising and unpredictable, they seem to
be patterned and constrained, at least with hindsight. What is the nature of the
patterns and constraints? What are the processes that underlie them?
If we think about stability, such as the stability brought about by tradition or
heredity, it is obvious that there must be mechanisms that resist change. Yes, environmental conditions can alter physiology and behaviour and these alterations
or their effects may sometimes be transmitted between generations, but if features are inherited it means that the system is not sensitive to every change in the
environment. What limits plasticity? What are the relations between stability and
plasticity, heredity and evolutionary change? Do we need to extend the concept
of plasticity?
The Sociological Review Monographs, 64:1, pp. 42–60 (2016), DOI: 10.1111/2059-7932.12012
C 2016 Sociological Review Publication Limited.
Published by John Wiley & Sons Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden,
MA 02148, USA
Cultural epigenetics
I pose these questions here (and will return to them at the end of the paper)
because there is a growing concern among social scientists and philosophers of
biology that the discussion around epigenetic inheritance is leading to a new type
of determinism. There is a tendency to identify inheritance, of whatever kind,
with a deterministic, rigid state of affairs that is not under developmental and
social control. Are we in danger of replacing genetic determinism with ancestralenvironmental epigenetic determinism?
One way of stopping the drift towards determinism while recognizing that
there are processes that can lead to persistence within and between generations is
to recognize the complexity of the dynamic, interacting and flexible processes that
go into the construction of a social system. Tavory et al. (2012, 2014) have suggested a developmental system approach to cultural dynamics that incorporates
this complexity that is inspired by Conrad Waddington’s cybernetic approach
to development and his developmental perspective of evolution. Waddington,
one of the founders of systems biology and the early proponents of what biologists now call evolutionary developmental biology (Evo-Devo), suggested a
visual metaphor, the ‘epigenetic landscape’, which depicted the embryonic development of animals as the progression of a ball through a sloping landscape
of alternative valleys (Waddington, 1957). Waddington was intrigued by the fact
that in spite of variation in genes and in developmental conditions, organisms
usually end up with a functioning, species-typical phenotype – a typically structured heart, a functioning eye, or a skilful locomotor ability. Waddington’s epigenetic (developmental) landscape was an attempt to illustrate how this came
about during embryogenesis. The epigenetic landscape describes ontogenetic development as a ball rolling down a tilted landscape, with many hills and branching valleys descending from a high plateau, which represents the initial state of
the fertilized egg. This landscape is shaped by underlying networks of interacting genes and their products, which dynamically respond to the developmental
environment and lead to a functional, usually species-typical, end state. As he
saw it, through natural selection acting on the genetic systems underlying it, the
landscape is mouded so that steep-sided valleys ensure that when development
is diverted away from its typical trajectory along the bottom of a valley, it either
returns to the valley bottom or, in extreme cases, shifts over into a different valley
(Figure 1).
Waddington called the stable maintenance of the trajectory of developmental
change homeorhesis, and he coined another closely related (and far more popular) term, canalization, to describe the process that brings about the relative
uniformity in the macroscopic phenotype. Canalization has been formally defined as ‘the adjustment of developmental pathways by natural selection so as
to bring about a uniform result in spite of genetic and environmental variations’
(Jablonka and Lamb, 1995: 290). In genetic terms it means that a typical phenotype is generated by many different underlying genotypes, in many different
environmental conditions. For example, in spite of the many genetic and environmental differences humans end up having a similar four-chambered heart.
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Figure 1 The epigenetic landscape. Top: the top of the landscape represents the
initial developmental state of the fertilized egg; the alterative descending paths are
some of the trajectories that can be followed during development. Bottom: the
complex system of interactions underlying the epigenetic landscape: black pegs
represent genes, and the guy ropes emanating from them represent the interacting
products of the genes. Figures 4 and 5 in Waddington (1957).
The mirror image of canalization is plasticity, which is usually defined as the
ability of a single genotype to generate variant forms of morphology, physiology, and/or behaviour in response to different environmental circumstances. The
response to new conditions can be reversible or irreversible, adaptive or nonadaptive, active or passive, continuous or discontinuous (West-Eberhard, 2003).
Sometimes the repertoire of plastic responses is limited and predictable, as, for
example, with seasonal changes in the colours and patterns that develop on butterflies’ wings, but it can also be open-ended and involve unpredictable, novel
responses, as seen when animals learn new behaviours through trial and error.
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Plasticity and canalization are intimately related (Jablonka, 2006). Processes
of canalization, which lead to stability in a ‘noisy’ world, must be based on the
capacity of underlying or overlying control systems to be adjustable and flexible,
so that the typical functioning phenotype can be constructed. Biochemical, neural and behavioural exploration can generate several alternative routes that all
end in the same dynamically stable state. For example, a robin’s nest can be built
in a hole in a tree stump, bank or wall, and near human habitation it will often
occupy old kettles, letter boxes, flower pots or hanging baskets. It can be made of
various types of leaves, grass and moss, and lined with roots or hairs. Where and
of what it is constructed depends on what is available to it, but the end result is a
typical robin nest in which it lays eggs. Canalization, therefore, necessarily implies
plasticity. Adaptive plasticity, on the other hand, requires that some processes are
canalized. The great variability of sentences in a natural language is based on the
canalized abilities of language-learners to attend to, imitate, remember and generate constrained sets of components and patterns of linguistic structure, and a
constrained range of phonemes that are organized in a combinatorial manner. It
is these canalized capacities that enable speakers to form theoretically unlimited
phoneme-strings and communicable meanings (Dor and Jablonka, 2010).
Social-cultural change is far more open-ended than the embryological
processes in animals that were Waddington’s main interest. However, Waddington’s depiction of networks of interactions that lead to stable states is a useful metaphor for describing social and cultural re-production. Tavory et al.’s
adaptation of Waddington’s descriptive model to social dynamics emphasizes
the regulatory interactions among the practices, institutions, schemas, epigenetic
predispositions, ecological affordances, and so on that lead to the continuous
reconstruction (with modifications) of the cultural landscape. An example is
the persistence over time of urban poverty in the US. The factors and processes
that lead to the reconstruction of poverty include the developmental effects of
malnutrition; the consumption of unhealthy food, alcohol or other toxins; poor
parenting; bad schools; limited job opportunities; residential segregation, the
low expectations of peers, parents, and teachers; outsiders’ prejudice, and so on.
These and other factors tend to sustain and reinforce the trajectories that lead
to poverty, and lead to the difficulty of escaping it. Another example is the reconstruction of Orthodox Jewish life in a Los Angeles neighbourhood, which
shows the interaction of numerous factors and processes that lead not only to
the persistence, but also the enlargement of this orthodox Jewish community,
whose members live surrounded by a non-Jewish ‘transgressive’ youth culture.
Among other factors, an educational system that demands significant parental
involvement, edicts regarding activities on the Sabbath, and the way in which Orthodox Jews are identified and self-identify, all contribute to the reconstitution of
the Orthodox Jews’ local culture (Tavory, 2016). Such a view of culture stresses
the importance of self-sustaining interactions among developmental-epigenetic
processes, familial interactions, and high-level social processes such as those occurring at the institutional level, and provides a way of incorporating information about political-historical events that have long-term self-reinforcing system
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effects, through processes such as historical trauma (Lock, 2015). As I describe
later, there is evidence suggesting that cultural practices lead to molecular epigenetic changes that in turn can contribute to the reconstruction of the system’s
dynamics.
The epigenetic link
Because the recent explosion of epigenetic research has resulted in many of the
basic terms being used inconsistently, throughout this paper I will use the definitions suggested by Jablonka and Lamb (2014: chapter 11).
The term epigenetics was originally coined by Waddington in the late 1930s
to describe the network of developmental interactions between genes and their
products that bring the phenotype into being (Waddington, 1968). Subsequently
the term evolved (Holliday, 1994; Jablonka and Lamb, 2002; Haig, 2004), and
today it is used mainly to describe the developmental changes associated with
cell heredity and cell memory. It has been used in both a broad and a narrow
sense: the narrow definition is focused on heritable changes in gene expression
that are not dependent on changes in DNA sequence, while the broader definition, which is that employed in this paper, includes additional aspects such
as cell memory. Epigenetics in this wide sense therefore describes ‘the study of
developmental processes in prokaryotes and eukaryotes that lead to persistent,
self-maintaining changes in the states of organisms, their components, and their
lineages’ (Jablonka and Lamb, 2014: 393).
At the cell level, epigenetic inheritance is said to occur when variations in information that are not determined by differences in DNA sequence are transmitted
to other cells. Information is usually transmitted vertically during cell division,
but it can sometimes also be transmitted horizontally between cells through the
movement of migrating molecules. It is important to distinguish between epigenetic inheritance that leads to the reconstruction of phenotypic states generation
after generation and repeated induction by the environment that can lead to a
particular phenotype being reconstructed. While the repeated or lingering environmental induction requires that the environmental inducing conditions are
repeated from one generation to the next, with epigenetic inheritance the original
environmental conditions need not be repeated because internal changes induced
in the organism’s physiology obviate the need for induction by the external stimulus (the external stimulus has been replaced by a persistent internal state). An example of repeated induction would be the induction by a consumed toxin of a new
phenotype, with this phenotype developing and persisting as long as the inducing
environment persists. With epigenetic inheritance on the other hand, exposure
to the toxin may occur for only a single generation, yet the effects of the toxin
may last many generations by inducing an internal self-reconstructing epigenetic
state, so that transmission of the variant phenotype occurs even if the original
external inducer is no longer present. Another case of epigenetic inheritance is
time-dependent accumulation of epigenetic marks that occurs even though the
external inducing conditions remain constant from one generation to the next.
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Developmental, context-sensitive changes in cellular information are brought
about by epigenetic mechanisms that establish and maintain changes in patterns of
gene expression and cellular structures in both non-dividing cells, such as mature
neurons, and in dividing cells such as stem cells. Four major types of mechanisms
have been recognized (reviewed in Jablonka and Lamb, 2014): (i) Self-sustaining
loops involving, for example, positive regulation of a gene’s activity by its products. Such positive regulation leads to the maintenance of a pattern of gene activity, and when the gene products are distributed during cell division, it leads to the
reconstruction of the same state of activity in daughter cells. (ii) Structural templating, in which three-dimensional cellular structures act as templates for the
production of similar structures, which may then become components of daughter cells. The templating involved in the propagation of prions is an example of
such a mechanism. (iii) Chromatin-marking, in which patterns of DNA modifications, such as the addition of methyl groups (CH3 ) to some cytosines and modifications in the histone proteins associated with DNA can be reconstructed during cell division. (iv) RNA-mediated systems, in which small non-coding RNA
molecules (ncRNA) regulate translation and transcription through interactions
with mRNA or DNA to which they are complementary. When transmitted, these
ncRNAs can affect translation and transcription in recipient cells.
One aspect of epigenetics that is receiving increasing attention is behavioural
epigenetics, which includes both the role of behaviour in shaping developmentalepigenetic states, and the reciprocal role of epigenetic factors and mechanisms
in shaping behaviour (Champagne and Rissman, 2011; Petronis and Mill, 2011;
Jablonka and Bronfman, 2014). The subject is of key importance for the study of
cultural epigenetics, but research into behavioural epigenetics is not confined to
human behaviour. Investigations of the epigenetic correlates of social behaviour
in animals have important implications for the study of animal behavioural ecology (Ledón-Rettig et al., 2013), and are also of major importance for students of
human culture because of the light they may shed on the (biochemically similar)
epigenetic basis of human behaviours.
There is now good evidence showing that through the mediation of epigenetic
mechanisms, lifestyle factors such as diet, smoking and alcohol consumption, as
well as familial and community psychological-sociological factors that modulate
disease risk, can affect not only the exposed individuals but also descendent generations (reviewed by Alegria-Torres et al., 2011; Párrizas et al., 2012). It is well
established that a mother’s diet during pregnancy influences the epigenetic profiles and phenotypes of her offspring (eg, Lillycrop et al., 2008; Choi and Friso,
2010), and that smoking (Bretonet al., 2009), excessive alcohol drinking (Hicks
et al., 2010; Hou et al., 2010), the use of addictive drugs such as cocaine (Vassoler
et al., 2013), and beneficial physical exercise (Zhang et al., 2011) are correlated
with changes in DNA methylation. In rodents, a single exposure of a pregnant
rat to the fungicide vinclozolin leads to significant deleterious alterations in the
physiology of her great-grandchildren (the F4 generation) (Anway, et al., 2005;
Guerrero-Bosagna and Skinner, 2012). The same seems to be true for dioxin, a
product of a wide range of manufacturing processes; for a hydrocarbon mixture
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used for dust control on road surfaces (jet fuel and JP8), and for plastics mixture
(eg bisphenol A, which many humans are exposed to daily and have traces of in
their urine; reviewed in Jablonka and Lamb, 2014). Three generations after rats
were exposed as fetuses to low doses of any of these compounds, the time of the
onset of puberty was altered and the rats had gonadal abnormalities. Each compound induced distinct changes in DNA methylation marks in the sperm. Bisphenol A has also been found to have transgenerational effects in mice. Adding it to
the food of female mice at a concentration that is comparable to that found in
humans had effects not only on the behaviour of the mice that were exposed while
in the uterus, but also on the behaviour of mice three generations later. The expression of a number of genes in the brain was changed in the exposed animals,
and some of these effects persisted into the fourth generation of descendants
(Wolstenholme et al., 2012). Psychological stress, too, has transgenerational effects: the offspring of male mice that were exposed to chronic stress either before
or after puberty had an altered HPA (hypothalamic–pituitary–adrenal) stress response and nine small non-coding RNA were expressed in their sperm under
these conditions (Rodgers et al., 2013).
In humans, a longitudinal study in the UK showed that the sons of fathers who
smoked before puberty (before they were 11 years old) had a shorter gestation
time and at 9 years of age had a greater body mass index (BMI) (Pembrey, 2010).
This probably means that the early-smokers’ sons will be at greater risk of obesity
and related health problems in adulthood. Even more strikingly, a Swedish study
showed that plentiful food supply in the paternal grandfathers’ mid-childhood
was associated with a four-fold increase in diabetes in the grandsons, while malnutrition of the grandfather was associated with increased longevity (Kaati et al.,
2002). In both humans and rodents, it has been found that a stressful or traumatic
experiences such as social defeat, a strong or enduring mental shock, physical and
emotional abuse, or deprivation of early parental care can have deleterious longterm, transgenerational effects that are mediated by molecular epigenetic mechanisms (Párrizas et al., 2012; Blaze and Roth, 2013; McGowan and Szyf, 2010).
The brain cells of humans are not accessible (except after death or during brain
surgery), so changes in their epigenetic state cannot be studied directly, but there
are correlated changes in the epigenetic state of genes in peripheral blood cells
and other non-neural tissues which can be more readily accessed (Uddin et al.,
2010; Mehta et al., 2013). Using blood cells, a study in Gambia found that individuals conceived during the nutritionally-stressful rainy season had significantly
higher methylation at several important gene loci than individuals conceived during the more plentiful dry season (Waterland et al., 2010; Dominguez-Salas et al.,
2014).
There are two main ways in which the epigenetic effects of behavioural or
lifestyle changes in the parents can be transmitted to descendants. First, epigenetic states can be reconstructed in the next generation through the direct effects
of altered parental physiology on their offspring’s development. This is what was
seen in some experiments Weaver and his colleagues (2004) carried out with rats.
They found that when a mother gave her biological or fostered offspring a low
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amount of licking and grooming, they had an increased stress response and neophobia. Crucially, when these biological or foster daughters themselves become
mothers, they also exhibited low licking and grooming behaviour, passed it on
to their daughters, and so on. These developmental changes were found to be
associated with epigenetic changes in DNA methylation and histone modification in the rats’ brains, which, although usually very stable, could be reversed by
administering drugs that affect chromatin structure (Weaver et al., 2005). This
is an example of epigenetic inheritance involving a self-sustaining loop between
the animal and its developmental environment: maternal behaviour → altered
brain physiology and epigenetic regulation in daughters (Epi1) → altered maternal behaviour in daughters → altered brain physiology and epigenetic regulation
in offspring, and so on.
The second way in which changes in parents can be transmitted to later generations is through the germline: epigenetic information is transmitted through the
gametes even when the gametes are not themselves exposed to the inducing factor. For example, the depression-like behaviour and anxiety of male mice, which
was the result of being deprived of normal maternal care for a few hours each
day for 14 days after birth, was transmitted through their sperm and persisted to
the F3 generation (Franklin et al., 2010; Gapp et al., 2014).
The mechanisms behind the transmission of the effects of behavioural and
lifestyle changes should become clearer now that the epigenetics of the nervous
system is being investigated. One of the striking discoveries of recent years is the
intimate involvement of epigenetic mechanisms in the establishment and maintenance of long-term learning and memory. Long-term memory is correlated
with gene-specific and genome-wide (global) changes in the neurons’ epigenome
(Blaze and Roth, 2013; Zovkic et al., 2013; Bronfman et al., 2014; in press). For
example, rats that learn to associate a certain experimental chamber with an electric shock (and freeze when they are introduced to it even when no shock is given)
undergo epigenetic changes in their hippocampal neurons: learning-facilitating
genes became demethylated, while learning-suppressing genes become methylated (Miller and Sweatt, 2007; Lubin et al., 2008; Miller et al., 2010). In addition
to such gene-specific epigenetic changes, there are also genome-wide effects. A
survey of the studies that have been made on the epigenetics of learning shows a
positive correlation between increased global levels of histone acetylation, DNA
methylation and learning. Furthermore, manipulation of the enzymes that enhance global histone acetylation or global DNA methylation also enhance the
strength and persistence of learning, while a decrease in these enzyme activities
decreases learning. These results appear to be consistent across taxa, developmental time, brain-region and learning task (Bronfman et al., 2014; in press).
Learning ability can be affected not just in the F0 generation that has been
exposed to stress or other conditions that affect learning ability – it can also
be carried over to the next generation. For example, exposure of domesticated
Longhorn chicken to stress not only hampered their own ability to learn, but
it also decreased the learning ability of their offspring, who were not themselves exposed to stress (Lindqvist et al., 2007; Nätt et al., 2012). Similarly,
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environmental enrichment, which can compensate for a learning-deficiency in
mutant mice, also improves learning in the F1 offspring that inherit the deleterious gene (Arai et al., 2009; Arai and Feig, 2011). More strikingly, some highly
specific effects of learning have been found to affect descendent generations beyond the F1 generation. Mice that were conditioned to associate a specific odour
(either acetophenone or propanol) with mild foot-shocks became startled when
they smelled the same odours in the absence of foot-shock. Remarkably, their
offspring and grand-offspring (the F1 and F2 generations) also responded with
a heightened startle-response to the odours to which their ancestors were conditioned (Dias and Ressler, 2014).
Finding that stress has transgenerational effects has obvious medical and epidemiological importance, but it also has social and political implications. If, for
example, long-lasting ethnic conflicts, starvation, or a persistently low socioeconomic status can induce detrimental cognitive and emotional effects in members of human populations, it could aggravate and reinforce social problems for
generations to come, because the epigenetic changes may lead to the reconstruction of the deleterious phenotypes. Recognizing persistent, socially induced deleterious effects that bias the reconstruction of similar conditions in descendants
will create an urgent need to understand how to manipulate the developmental
system and neutralize or reverse those effects.
Reciprocal interactions between the social and epigenetic systems?
In humans, food habits, the type and extent of physical exercise, sexual behaviours, the degree and type of familial care and social stresses, are both
consequences and causes of cultural practices and carry cultural meaning. For
example, what is considered shameful and hence stress-inducing varies between
cultures. The human social system not only constructs persistent life-styles, but
also imbues them with symbolic meaning and psychological-social value.
The study of social and cultural epigenetics is still in its infancy, so we do not
have detailed studies of the relations between socio-cultural conditions and epigenetics. It is well established, however, that social inequality (eg, poverty) in geographically, politically, and economically diverse populations is correlated with
an increased risk of cardiovascular diseases, cancer and psychological disorders,
and that all these deleterious conditions have epigenetic underpinnings (reviewed
and discussed by Thayer and Kuzawa, 2011; Hicks and Leonard, 2014; Lock,
2015). The disposition to develop such deleterious effects can be transmitted to
the next generation and contribute to the difficulty of escaping poverty. To break
away from this vicious cycle political-social action is needed alongside the search
for new treatments that can compensate for and reverse the adverse persistent
epigenetic effects.
Wars, like chronic poverty, have multiple effects leading to both nutritional
and psychological stresses. Individuals who were conceived during the severe
food shortage of the Dutch Hunger Winter at the end of World War II, when the
Nazi occupiers cut daily food rations to less than 700 kcal, 60 years later suffered
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from problems such as an increased risk of diabetes, obesity, schizophrenia and
coronary disease (Heijmans et al., 2008). Compared with siblings of the same sex
who were born during better times, they showed widespread differences in DNA
methylation patterns, including at the insulin-like growth factor 2 (IGF2) locus.
Wars also have long-term psychological effects, and there are indications that
war-related stress can affect descendants’ disposition to develop trauma-related
vulnerabilities. For example, the children of Holocaust survivors are more prone
to develop post-traumatic stress disorder (PTSD) than control groups, and even
the short stress of the September 11th attack seems to have led to behavioural
changes in the children of women who were pregnant while witnessing it (Yehuda
and Bierer, 2009; Sarapas et al., 2011). Indeed, changes in the methylation
of the glucocorticoid promoter, a DNA region controlling stress sensitivity,
that are associated with parental PTSD and their children’s vulnerability to
trauma were found in Holocaust survivors (Yehuda et al., 2014). More recently,
between-generational effects on the methylation of an important regulator
of GR-sensitivity, FKBP5, which have been associated with both PTSD and
intergenerational effects, have been demonstrated, showing a direct (inverse) relationship between induced methylation marks in traumatized parents and their
descendants’ methylation profile (Yehuda et al., 2015). As Lock has emphasized,
to understand human bodies and biologies we must consider the historicalpolitical realities of social lives, for humans are bio-socially becoming beings.
For example, the study of the effects of historical traumas undergone by Inuit
communities in Canada is necessary for understanding the past, present and
future of these communities, at all levels – from the symbolic to the epigenetic
(Lock, 2015).
As yet there are no studies that have teased apart the various ways in which
the psychological stresses of war could affect people’s descendants. Psychological stresses can have different effects in the next generation, including stresscompensating effects, but we do not know what the trade-offs (if there are any)
between such resilience and other traits are. The severity and transmissibility of
the effects of war stresses may depend on the extent and duration of parental
stress and on subsequent, post-natal conditions. When the effects of war stresses
are transmitted to descendants, we need to know for how many generations they
persist, and whether they are caused by changes that occur in the gametes of the
parents, in the uterine environment, in the way infants were nursed, in the way
that children were brought up, or a combination of these factors. For example, a
distinction between epigenetic gametic inheritance and lingering or repeated direct induction of epigenetic variations requires that the F2 (second-generation)
offspring of affected males and F3 (third generation) of exposed females must be
tested: persistently altered epigenetic variations in these descendent generations
would be evidence for epigenetic inheritance (Jablonka and Raz, 2009).
Another important set of processes must be added to this web of entanglements: it is not the genome or the epigenome of people alone that needs to be
considered but also the genome and epigenome of the microbes they carry and,
of course, the web of interactions between them. There is a growing body of data
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pointing to the reciprocal interactions between physiological and mental stress,
epigenetic effects and the microbiome – the microbes that live inside and on us
(Gur et al., 2015). It is plausible that the brain and behaviour-related effects of
the microbiome (Galland, 2014) have transgenerational effects, both through the
transmission of the microbiomic profiles (Gilbert and Epel, 2015) and through
the epigenetic effects induced by it.
In spite of all these complications, the investigation and characterization of
the epigenetics of historical trauma is not an impossible endeavour, although
studying these effects requires an intense interdisciplinary effort and good health
records spanning many years. Such studies may reveal not only the persistent
epigenetic effects of warfare and their interactions with psychological and social
factors, but also whether the epigenetic effects wrought by wars contribute to or
decrease the risk of future domestic and social conflicts – for example, whether
they predispose the offspring of victims to be more stress-sensitive, aggressive or
averse to aggression under adverse conditions.
Human cultural evolution: a role for epigenetic anthropological
and historical studies
Understanding the epigenetics behind the interplay between individual and social behavior, the epigenetic differences associated with conditions of chronic,
self-perpetuating poverty, the changes brought about by acute and chronic war
conflicts, persistent pollution, or persistent gender-specific trauma (female genital mutilation) are, of course, of urgent political importance and present huge
methodological problems. But there are other less socially pressing problems
that are of great interest to social scientists and biologists. Human populations
have very different local cultures: they differ in their food preferences, in the way
men and women live and are treated, where they choose to live and their type of
dwelling, in the way they care for their children, and so on. All of these persistent cultural traditions are likely to have epigenetic correlates, and diet-related
cultural variations will have additional correlated changes on the constitution of
the microbiome of group members (Yatsunenko et al., 2012; Kau et al., 2013).
The epigenetic profiles and the microbiomes of different human cultural and
social and gender groups within a culture may be more shared than their genetic profile, and can be closely related to symbolic and institutional aspects of
the culture, both reflecting and driving changes in cultural practices. For example, migration to new areas where a different culture is dominant, can lead to
far-reaching changes in the epigenetic profile of migrant descendants, although
some groups may preserve particular aspects of their life style and these can affect
the host population and alter its epigenetic profile. In other words, a change in
the social landscape is likely to involve a change in the epigenetic landscape. This
includes changes in the microbiome that participate in developmental processes
that lead to persistent, self-maintaining changes in the states of the host organisms, and is therefore, by definition, part of the epigenetic system (Gilbert and
Epel, 2015). The study of the epigenetic constitution and the microbiomes of
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human cultural groups and their relation to the persistent and changed social
landscape that humans inhabit is an exciting new research area.
Comparisons of present-day human cultural groups would probably include
three or even four generations of people, sometimes living under differing conditions (eg, following migration or other significant cultural changes), but this
does not exhaust the potential of epigenetic-cultural research. Techniques are
now available that enable biologists to study differences in DNA methylation in
long-dead animals and even in long-extinct species. The first such study was of the
remains of the late-Pleistocene steppe bison (Bison priscus), and it showed that
methylation patterns are preserved in ancient DNA and can yield information
about the methylomes of extinct animals (Llamas et al., 2012). A recent study
of the methylomes of Neanderthals, Denisovans and present-day Homo sapiens
identified around 2,000 differentially methylated regions in archaic and presentday humans, some of which are related to genes associated with anatomical differences and diseases. These findings suggest that epigenetic variations may have
been one of the many factors driving hominid evolution (Gokhman et al., 2014).
In addition, recent comparison of the fossilized faeces (coprolites) in Huecoid
and Saladoid cultures from a settlement on Vieques Island, Puerto Rico, showed
that the two cultures can be distinguished from each other on the basis of their
bacterial and fungal gut microbiomes (Cano et al., 2014). I believe that these
new molecular techniques open up the possibility of epigenetic studies of human
history (on any chosen time scale). Such studies could be based on the analysis
of DNA methylation in the bones or other DNA-containing human remains, as
well as the DNA of coprolites in different periods and areas. The epigenetic findings would add new and important information about the social-cultural lives
of dead people and cultures, enriching and extending historical, anthropological
and archaeological research. The epigenomes of populations with different cultural tradition that lived in the same historical period could be compared, and
the epigenetic profiles of cultural groups could be followed over timespans of
hundreds and thousands of years.
The study of human epigenetic evolution could also contribute to our understanding of their genetic evolution. Genetic evolution during historical times was
relatively rapid after the last ice age, 40,000 years ago, when it was driven by environmental fluctuations, population growth, and the colonization of new areas
(Hawks et al., 2007; Wills, 2011). However, it was probably much slower than epigenetic evolution: epigenetic variations are generated in an environmentally sensitive manner and at a much greater rate than genetic variation. Since genetic and
epigenetic variations interact, the more rapid epigenetic variations could drive
genetic evolution. The domestication of animals, a very rapid evolutionary process, seems to involve both genetic and epigenetic variations (Nätt et al., 2012;
Jablonka and Lamb, 2014), and although we know very little about the interactions between these two types of variations, systematic comparative studies of
domesticates and their wild ancestors could remedy this deficiency. Such studies would enrich research in animal behavioural ecology (Jablonka, 2013) and
may have implication for the study of human evolution. If social selection for
The Sociological Review Monographs, 64:1, pp. 42–60 (2016), DOI: 10.1111/2059-7932.12012
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Eva Jablonka
increased cooperation and communication within human groups was a factor in
human evolution, it may have led to increased executive control of emotions, to
the promotion of social emotions (Jablonka et al., 2012) and to a more docile
and affable behaviour within groups. Such behavioural and cognitive changes
have epigenetic correlates that could have influenced and accelerated what some
people see as a form of human self-domestication (Brüne, 2007).
Although extracting DNA from bones of dead humans may require digging
up people’s graves, which might offend some religious sensibilities, it could open
up fascinating vistas of human history and biology. I predict that this type of
historical-epigenetic research will become an important and intensely researched
topic in the near future, a new tool in the historian’s toolbox.
Conclusions
Meloni (2014a) has discussed the way in which epigenetics research seems to
be leading to the exaggerated view of epigenetic variation as the key to human
nature, and the fear that epigenetics will promote a new kind of simplistic environmental determinism with no place for human agency. It is of course always
difficult to avoid over-interpreting new path-breaking discoveries, and the attention given to findings made in epigenetic research is certainly a recent example of
this tendency. Epigeneticists who study the relation between people’s epigenetic
marks and their past and present life experiences understandably highlight those
findings that suggest that environmentally induced epigenetic differences can
make significant hereditary differences. Moreover, because of the old dogma that
identifies hereditary variations exclusively with genetic variations, and maintains
that developmentally acquired variations cannot be inherited, young biologists
have become excited about the evolutionary implications of robust epigenetic
inheritance. Given these reactions to epigenetics and epigenetic inheritance, it is
almost inevitable that especially in the pens of simple-minded popularizers the
significance of the results of epigenetic research (like those of genetics in the not
too distant past) is sometimes exaggerated and misinterpreted.
In contrast, epigenetics may generate concerns amongst social scientists, who
are wary of attempts to biologize culture and regard any mention of a biological
approach to culture as carrying the threat of simplistic reductionism and distrust
any bio-social talk (Meloni, 2014b). For example, social scientists worry that epigenetic inheritance can be seen as marking individuals in disadvantaged groups
that were exposed to a particularly bad environment such a chronic starvation
or chronic psychological stress with ‘bad (epigenetic) heredity’. This is the gist of
the argument that the acceptance of Lamarckian inheritance can lead to a belief
in biological inequality based on the inheritance of the deleterious effects of social deprivation, the fallacious argument that: ‘centuries of poverty, ignorance,
disease, and oppression should have ingrained a most undesirable heredity upon
the vast majority of the human species, and engrained it so firmly that a few generations of improved conditions could not be expected to effect much amelioration’ (Huxley, 1949: 187). This argument is based on the assumption that such
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Lamarckian inheritance is irreversible, and that over time, as the deleterious acquired variations accumulate, they become more stable and ‘engrained’. These
assumptions may often be unwarranted. First, as the many studies on the effects
of the environment on epigenetic variations show, new inducing conditions, such
as exposure to specific nutrients during sensitive developmental periods, alter existing epigenetic marks, so epigenetic marks are not written in stone. Second, even
when epigenetic variations accumulate over time in an inducing environment and
can be selected, they may be reversed when the environment changes. Cropley and
her colleagues (2012) have shown that combining methyl donor supplementation
with selection for a silent Avy allele, progressively increases the prevalence of the
associated phenotype in the population over five generations, but that once the
supplementation is removed there is reversion to the original epigenetic state (in
the F0 generation). Hence, epigenetic marks can be reversed although we do not
always know how to reverse them, and scientists cannot ensure that the relevant
scientific knowledge will not be ignored or misused. But even as the realization
that the history of the individual matters in subtle and surprising ways grows, social epigenetic research must also explicitly incorporate political and social levels
of analysis, for it is these levels that determine the way in which the data is classified, and the way data sets are compared. Epigenetic responses are sensitive
to the differences between men and women, between different social classes and
between different ethnic communities.
I believe that in spite of the present media hype around epigenetics and the understandable concerns of social scientists, epigenetics is forming a natural meeting point between the biological, the social sciences and the humanities, and
the interaction among the disciplines is likely to intensify as new techniques
for deciphering the ancient epigenomes become available. At the conceptual
level, acknowledging the existence of epigenetic inheritance renders the classical
nature-nurture dichotomy obsolete, because it means that heredity (‘nature’) can
be developmentally constructed (‘nurtured’). The ‘biosocial’ entails reciprocal interactions between biological and sociological factors, showing, in this case, both
how social processes impact epigenetic ones and how epigenetic effects impact the
social for both the directly induced generation and for descendent generations.
One can, therefore conceptualize epigenetic inheritance in terms of temporally
extended plasticity: developmentally induced epigenetic changes can be heritable for few or many generations, and plasticity can therefore have a temporal
(hereditary) dimension, which blurs the distinction not only between ontogenetic
plasticity and heredity, but also between plasticity and evolvability (Lamm and
Jablonka, 2008). Furthermore, since epigenetic variations are both causes and
effects of developmental changes, they have to be understood in terms of dynamic networks of interactions and not in terms of single epigenetic variants.
Finally, it must be recognized that when changes in epigenetic variation occur,
often as a result of a change in conditions, they alter developmental dispositions,
not characters. What is changing when environmental conditions change is the
shape of plasticity: plasticity, including hereditary plasticity, is not compromised
but is itself plastic. These theoretical points are fleshed out when we think about
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culture in Waddingtonian terms. A close scrutiny of any social-cultural landscape shows that it exhibits both canalization and plasticity and is the outcome
of reciprocal and flexible relations among multiple biological and social-cultural
resources that affect the life-trajectories of individuals (their biosocial becoming, to use Lock’s perspicacious term) and shape group-level dynamics. Such a
developmental-system view of culture, is, I believe, a good antidote to the biologization of culture by some biologists and may abate the bio-anxiety of social
scientists. It makes clear that the political, the ideological and the biological are
deeply entangled.
Acknowledgements
I am very grateful to Marion J. Lamb for her invaluable contribution to every aspect of this paper, and to the referees for their helpful and thoughtful comments.
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