Epigenetics in psychology

Epigenetics in psychology helps to explain how nurture shapes nature, where nature refers to biological heredity and nurture refers to virtually everything that occurs during the life-span (e.g., social-experience, diet and nutrition, and exposure to toxins). Epigenetics in psychology provides a framework for understanding how the expression of genes is influenced by experiences and the environment to produce individual differences in personality, behaviour, cognition and mental health.

The subdiscipline of behavioral epigenetics is the field of study examining the role of epigenetics in shaping animal (including human) behaviour. Epigenetic gene regulation involves changes other than to the sequence of DNA and includes changes to histones (proteins around which DNA is wrapped) and DNA methylation. These epigenetic changes can influence the growth of neurons in the developing brain as well as modify activity of the neurons in the adult brain. Together, these epigenetic changes on neuron structure and function can have a marked influence on an organism's behavior.

Discovery

The first documented example of epigenetics affecting behavior was provided by Meaney and Szyf. While working at McGill University in Montréal in 2004, they discovered that the type of mothering a rat receives in infancy determines how that rat responds to stress later in life. Rat pups that receive a less nurturing upbringing are more sensitive to stress throughout their life span. This stress sensitivity is linked to a down-regulation in the expression of the glucocorticoid receptor in the brain. In turn, this down-regulation was found to be a consequence of the extent of methylation in the promoter region of the glucocorticoid receptor gene. This pioneering work in rodents has been hard to replicate in humans because of a general lack of human brain tissue for measurement of epigenetic changes. The first study that has directly linked epigenetic changes in human brain tissue to behavior involved post-mortem brains of people who committed suicide, half of whom had been abused as children. Those who had been abused had a lower expression of glucocorticoid receptor due to increased methylation in the promoter region of the glucocorticoid receptor gene. These observations in humans closely parallel the earlier rat studies.

Background

History

For more details on this topic, see Epigenetic etymology and definitions.

British biologist Conrad Waddington is credited with developing the term epigenetics in 1947. Epi is a Greek term meaning upon or above. Hence, epigenetics reflects the effects that take place upon, above or in addition to genetics. This original definition implied that something aside from genes was involved in defining the phenotype. When Waddington created the term epigenetics, little was known about the expression of genes. Waddington and others eventually realized that development involved networks of interactions between genes. By the 1990s, Hall wrote that epigenetics involves genetic and non-genetic factors that affect gene expression. Hall further noted that the code of heredity includes an extra layer in addition to DNA. By the 2000s, epigenetics was used to describe how experiences shape heritable genetic expression. Psychosocial and environmental factors have been shown to alter these epigenetic mechanisms which, in turn, influence normal and abnormal psychology. The current definition still maintains its continuity to Waddington’s, as epigenetics is used to explain how genes and the environment work in tandem. However, epigenetic changes do not alter or mutate the DNA. Instead, epigenetic mechanisms affect DNA by regulating the expression of genes. Therefore, due to their regulatory function, epigenetic mechanisms are still considered to occur upon or above the DNA without actually altering it.

Epigenetic mechanisms

Main article: Epigenetics

Modifications of the epigenome do not alter DNA.

Two of the best understood mechanisms of epigenetic modification include DNA methylation and histone modification. DNA methylation, the best understood epigenetic modification, results in the inability of genetic information to be read from DNA. In other words, epigenetic modification can "turn off" a gene. This mechanism of turning off genes is reversible.

Genes can be likened to books, categorized and arranged, in a library. The books contain enormous amounts of accessible information that can be utilized in an infinite number of ways. Therefore, books are similar to DNA in that both are “waiting to be read.” In a library, many factors may contribute to whether a book will or will not be read. If a book is difficult to reach or being blocked by a piece of furniture, the book may not be read. Like an unread gene, an obstructed book is not altered or discarded. Both are still present, but if they are not accessible, neither the gene nor the book can be read. In this manner, epigenetics can silence a gene.

Genes contained within DNA constitute a complete instruction set. Epigenetics, in part, controls if and when these individual genes are expressed. The epigenome, a set of chemical markers attached to the DNA, is a secondary code that acts like a referee in activating and de-activating genes. Hence, epigenetics has a strong influence on the development of an organism and can alter the expression of individual traits.

Epigenetics across the life-span

Epigenetic changes occur not only in the developing fetus, but also in individuals throughout the human life-span. Increased levels of epigenetic changes have been found in older monozygotic ("identical") twins than in younger twins. Since identical twins become more epigenetically dissimilar as they age, epigenetic changes occur cumulatively over the life-span. Epigenetic changes, affecting the regulation of gene expression, are also reversible.

Inheritance

Epigenetic modifications can also be inherited from one generation to the next. Specifically, the effects of epigenetics may be transmitted from parents to children through meiosis and mitosis - processes that pass genetic information from the father into the sperm and from the mother into the egg. Hence, subsequent generations may be affected by the epigenetic changes that took place in the parents. Epigenetic modifications in offspring, resulting from parental environments, may also be passed down from generation to generation. Epigenetic research counters the long-standing notion that children are born with an uncontaminated genetic slate.

Comparison with evolution

According to Darwin’s classic theory of evolution, several generations are required for adaptation to occur. Also known as natural selection, this process contributes to humans' (and other species') ability to survive and reproduce in their particular environments. Adaptation may occur through physiological, structural (anatomical) and/or behavioural changes. In the context of natural selection and psychology, more successful (i.e., better adapted) traits and behaviours are more likely to be passed down from an individual to subsequent generations. Thus, most evolutionary psychologists agree that modern human traits and behaviours can be characterized as beneficial adaptations to the environment. However, other theorists argue that some traits are maladaptive. Not to be confused with evolution, epigenetics provides a mechanism for immediate adaptations to ever-changing environments throughout the human life-span.

Individual diversity, stemming from epigenetic differentiation, cannot be attributed to random mutations. Therefore, one view suggests that epigenetics is inconsistent with Darwinian theory of evolution’s concept of random mutations resulting in diversity. Although Lamarckism is not appropriate to explain evolution, it might offer insight into epigenetic-related individuation. Evolutionary developmental biology, for example, accounts for epigenetic and pseudo-Lamarckian mechanisms whereby environmentally induced variation is inherited. Another view maintains that epigenetics can be accomodated within a neo-Darwinian framework. In this context, inheritable epigenetic differences are viewed as part of long-term development, whereby the number of generations through which epigenetic modifications traverse is dependent on the duration of the influence on the genes.

Personality

Anxiety and risk taking

Monozygotic Twins are identical twins. Twin studies help to reveal epigenetic differences related to various aspects of psychology.

Epigenetic differences have been linked to differences in risk-taking and reactions to stress. Specifically, epigenetic differentiation in monozygotic twins has been shown to play a role in individual differences in:

• risk-taking that is characterized by impulsive or disinhibited decision making.
• the levels of anxiety (a state of apprehension or fear that arises during stress) and somatic complaints (physical ailments, symptoms and/or pain in the absence of underlying medical conditions – usually associated with anxiety). Anxiety and somatic complaints have been associated with the broad personality trait of neuroticism.

Epigenetic variations, associated with risk-taking behaviours and anxiety, have been linked to individual differences in lifestyle and career choices. In one study, each member of a pair of twins had chosen two very different life paths. One twin, who displayed high-risk behaviours (like gambling), chose a dangerous and high-sensation career as a war journalist. Despite the dangerous profession, this twin showed no elevated anxiety levels when confronted with stress. This twin married late in life (to an individual who also chose a dangerous profession), had no children, and consumed more alcohol than is considered medically healthy. In contrast, the other twin was considered to be a polar opposite. The second twin was prone to anxiety and developing somatic complaints when faced with stress. Instead of displaying risk-taking behaviours, the second twin displayed risk-averse behaviours. The second twin chose a safe and predictable career as a manager in a law firm, married a lawyer, had children at a young age and had only traveled out of country once (to another English-speaking country).

In this twin study, epigenetic differences in DNA methylation of the CpG islands proximal to the DLX1 gene have been implicated as affecting risk-taking behaviours and coping with stress in terms of anxiety. DLX1 exerts its effects by helping to regulate the production of the neurotransmitter GABA (gamma-aminobutyric acid), and the hormone neuropeptide Y. GABA decreases stress by acting on what is often referred to as the stress centre of the brain - the hypothalamic-pituitary-adrenal axis, or HPA axis. Conversely, neuropeptide Y negates the effect of GABA on the HPA axis and results in an increased stress response. In general, activation of the HPA axis, as part of the stress response, has been well-established in resulting in increased anxiety and depression. The epigenetic differences pertaining to GABA and neuropeptide Y, and their associated physiological HPA processes, have been posited to help explain individual differences in risk-taking behaviour and anxiety. In turn, this helps to explain why one twin functioned without anxiety under extremely dangerous situations.

Despite the associations between epigenetic markers for individual differences in personality traits and behaviours that might influence occupational choices, epigenetics cannot, on their own, predict complex decision-making processes like career choices. Such complex decisions transcend genetic predication.

Stress

The hypothalamic pituitary adrenal axis is involved in the human stress response.

The early parental-caregiving environment has long been a central focus of human psychological development. Early abuse and neglect can lead to a wide range of cognitive and emotional impairment. Animal studies reveal that the influence of early maternal care also affects genetic expression. In their review of a series of studies, Szyf, McGowan and Meaney indicated that early maternal care affected offspring's reactivity to stress. Specifically, the effects of maternal care, in terms of the parental licking-grooming of offspring, were examined. High licking-grooming resulted in a positive, long-term effect on the reactivity of the HPA axis when compared to pups who received low levels of licking-grooming. This was evidenced by decreased adrenocorticotropic hormone (ACTH) and corticosterone in response to stress in offspring. The effects of parental care on the HPA and ACTH resulted from epigenetic changes, whereby high licking-grooming led to decreased DNA methylation. This allowed for increased access to the hippocampal glucocorticoid receptor genes in the offspring. Increased expression of hippocampal glucocorticoid receptors causes the hippocampus to release less ACTH-releasing hormone, which acts on the pituitary gland to release less ACTH, which in turn acts on the adrenal glands to release less cortisol. In contrast, less parental care (low licking-grooming) ultimately results in increased cortisol release. The release of increased cortisol, via the HPA axis, as a reaction to psychological stress is well-established. Therefore, pups that received less licking-grooming were more prone to react to stress. Since humans also show the same cortisol response to stress and heritable cortisol levels, the animal models have implications for humans.

Research has also demonstrated that the maternal genotype did not determine stress reactions in offspring. Instead, the early parental care environment affected genetic expression to influence how offspring react to stress. When rat offspring were removed from their low licking-grooming mothers and placed with high licking-grooming mothers, the epigenetic changes related to an increased stress response were reversed. The reverse was observed when pups were removed from their high licking-grooming parents and placed with low licking-grooming mothers. This research provides evidence for an underlying epigenetic mechanism, as the stress response in offspring was determined by the foster mother, not the biological, genetic mother.

Research has also demonstrated the reversibility of epigenetic changes related to maternal care in mice. When adult offspring of low licking-grooming mothers were injected with an agent that decreased DNA methylation to match levels of adult pups of high licking-grooming mothers, their responsivity to stress decreased to match the levels seen in the offspring of high licking-grooming mothers. Conversely, when adult offspring of high licking-grooming mothers were injected with an agent to increase DNA methylation, their response to stress increased to match adult offspring of low licking-grooming parents.

Stable epigenetic variations in parental care can be passed down from one generation to the next, from mother to female offspring. Female offspring who received increased parental care (i.e., high licking-grooming) became mothers who engaged in high licking-grooming. Conversely, offspring who received less licking-grooming became mothers who engaged in less licking-grooming. Research has also provided the transgenerational epigenetic link related to maternal care. To this end, offspring of mothers with high licking-grooming behaviour evidenced DNA methylation-related increased expression of an estrogen receptor gene in the medial preoptic region of the hypothalamus – an area of the brain known to be linked to maternal nurturing and care.

In humans, the relationship between prenatal exposure to maternal mood and genetic expression resulting in increased reactivity to stress in offspring has been confirmed. Three groups of infants were examined: those born to mothers medicated for depression with serotonin reuptake inhibitors; those born to mothers not being treated for depression; and those born to non-depressed mothers. Prenatal exposure to depressed/anxious mood was associated with increased epigenetic changes in terms of increased DNA methylation at the glucorticoid receptor gene. In turn, this was related to increased HPA axis stress reactivity - as measured by increased salivary cortisol - in three month old infants. Research has well-established that increased cortisol levels are associated with increased stress. The findings were independent of whether the mothers were being pharmaceutically treated for depression.

Cognition

Learning and memory

Evidence shows that the environment exerts an influence on epigenetic changes related to cognition, in terms of learning and memory. Animal studies using mice with extensive neurodegeneration and synaptic loss in the forebrain indicated that environmental enrichment helped to restore spatial learning and long-term memories. Specifically, mice with brain damage were subjected to a fear paradigm that consisted of a single exposure to a conditioning context followed by an electric foot shock that elicited a freezing (i.e., staying still) response. After training, the mice were allowed to rest for four weeks in order to develop long-term memories. Mice were then housed in regular animal cages or in an enriched environment for ten weeks. The enriched environment consisted of cages with running wheels, play tunnels, and climbing apparatuses. When re-exposed to the conditioned context, mice housed in regular cages displayed impaired freezing responses. Conversely, the environmentally-enriched mice displayed the freezing behaviour, indicating a recovery of long-term memories.

Other memory-related research has yielded similar results. For example, when placed in a tub of water, brain-damaged mice learned to swim to a platform to escape from the water in the Morris water navigation task. After training, the brain-damaged mice that had resided in regular cages could not swim directly to the platform. However, brain-damaged mice living in an enriched environment were still able to remember where the platform was located by swimming to it – indicating a recovery of long-term memories. The environmental enrichment induced epigenetic changes in the hippocampus and cortex regions (via histone acetylation) of the brain. Injection of histone deacetylase inhibitor was shown to increase hippocampal acetylation and mimic the effects of environmental enrichment in brain-damaged rats. This was apparent through reinstating learning and a reduction in long-term memory loss related to the freezing-fear response and performance on the Morris water maze. These findings are consistent with human studies that have noted fluctuations in cognition, including temporary periods of clear memories, in individuals with dementia. Research has also linked learning and long-term memory formation to reversible epigenetic changes in the hippocampus and cortex in animals with normal-functioning, non-damaged brains. In human studies, post-mortem brains from Alzheimer patients show increased histone de-acetylase levels.

Animal studies have also provided evidence for epigenetic, age-associated memory decline. Older mice show increased epigenetic changes (i.e., decreased histone acetylation and reduced gene expression) in the hippocampus that is related to poorer learning and memory in the Morris water maze. Specifically, older mice spend more time to find the platform and escape from the water. Agents used to increase histone acetylation (i.e., reverse the age-related epigenetic effects) lead to improved performance in the older rats.

One review also noted the role of DNA methylation in memory formation and storage, but the precise mechanisms involving neuronal function, memory, and methylation reversal remain unclear.

Psychopathology and mental health

Substance use and addiction

Environmental and epigenetic influences seem to work together to increase the risk of addiction. For example, environmental stress has been shown to increase the risk of substance use. Specifically, in an attempt to cope with stress, alcohol and drugs can be used as an escape. Once substance use commences, however, epigenetic alterations may further exacerbate the biological and behavioural changes associated with addiction.

Even short-term substance use can produce long-lasting epigenetic changes in the brain, via DNA methylation and histone modification. Epigenetic modifications have been observed in studies using alcohol, nicotene, cocaine, amphetamines, and opiates. Specifically, these epigenetic changes modify gene expression. In turn, this increases the vulnerability of an individual to engage in future, repeated substance use and even greater epigenetic changes in the brain's pleasure-reward areas (e.g., in the nucleus accumbens). Hence, a cycle emerges whereby changes in the pleasure-reward areas contribute to the long-lasting neural and behavioural changes associated with the increased likelihood of addiction, the maintenance of addiction and relapse. For example, in humans, alcohol consumption has been shown to produce epigenetic changes that contribute to the increased craving of alcohol. As such, epigenetic modifications may play a part in the progression from the controlled intake to the loss of control of alcohol consumption. These alterations may be long-term, as is evidenced in smokers who still possess nicotine-related epigenetic changes ten years after cessation. Therefore, epigenetic modifactions may account for some of the behavioural changes generally associated with addiction. These include: repetitive habits that increase the risk of disease and personal and social problems; need for immediate gratification; high rates of relapse following treatment; and the feeling of loss of control.

Evidence for related epigenetic changes have come from human studies on alcohol, nicotine and opiate use. Evidence for epigenetic changes stemming from amphetamine and cocaine use derives from animal studies. In animals, drug-related epigenetic changes in fathers have also been shown to negatively affect offspring in terms of poorer spatial working memory, decreased attention and decreased cerebral volume.

Eating disorders and obesity

Epigenetics help to facilitate the development and maintenance of eating disorders via influences in the early environment and throughout the lifespan. Pre-natal epigenetic changes due to maternal stress, behaviour and diet may later predispose offspring to persistent, increased anxiety and anxiety disorders. These anxiety issues can precipitate the onset of eating disorders and obesity and persist even after recovery from the eating disorders.

In addition, epigenetic differences may accumulate over the life-span, thus accounting for the often incongruent differences in eating disorders observed in monozygotic twins. At puberty, sex hormones may exert epigenetic changes (via DNA methylation) on gene expression, thus accounting for higher rates of eating disorders in men as compared to women. Overall, epigenetics contribute to persistent, unregulated self-control behaviours related to the urge to binge.

Schizophrenia

Epigenetic changes, including hypomethylation of glutamatergic genes (i.e., NMDA-receptor-subunit gene NR3B and the promoter of the AMPA-receptor-subunit gene GRIA2) have been observed in the post-mortem human brains of schizophrenics. These are associated with increased levels of the neurotoxin glutamate. Since glutamate is the most prevalent fast excitatory neurotoxin, increased levels have been noted to result in the psychotic episodes related to schizophrenia. Interestingly, epigenetic changes affecting a greater number of genes have been detected in men with schizophrenia as compared to women with the illness.

Population studies have also established a strong association linking schizophrenia in children to older fathers. Specifically, children born to fathers over the age of 35 years are up to three times more likely to develop schizophrenia. Epigenetic dysfunction in human male sperm cells, affecting numerous genes, have been shown to increase with age. This provides an explanation for increased rates of the disease in men. To this end, toxins (e.g., air pollutants) have been shown to increase epigenetic differentiation. Animals exposed to ambient air from steel mills and highways show drastic epigenetic changes that persist after removal from the exposure. Therefore, similar epigenetic changes in older human fathers is likely. Further, schizophrenia studies provide evidence that the nature versus nurture debate in the field of psychopathology should be re-evaluated to accommodate the concept that genes and the environment work in tandem. As such, many other environmental factors (e.g., nutritional deficiencies and cannabis use) have been proposed to increase the susceptability of psychotic disorders like schizophrenia via epigenetics.

Bipolar disorder

Evidence for epigenetic modifications for bipolar disorder is unclear. One study found hypomethylation of a gene promoter of a prefrontal lobe enzyme (i.e., membrane-bound catechol-O-methyl transferase, or COMT) in post-mortem brain samples from individuals with bipolar disorder. COMT is an enzyme that metabolizes dopamine in the synapse. These findings suggest that the hypomethylation of the promoter results in over-expression of the enzyme. In turn, this results in increased degradation of dopamine levels in the brain. Further, these findings provide evidence that epigenetic modification in the prefrontal lobe is a risk factor for bipolar disorder. However, a second study found no epigenetic differences in post-mortem brains from bipolar individuals.

Limitations and future direction

Many researchers are contributing information to the Human Epigenome Consortium. The aim of future research is to reprogram epigenetic changes that will help with addiction-related issues, mental illnesses, age related changes and memory decline. However, the sheer volume of consortium-based data makes analysis difficult. Most studies also focus on one gene. In actuality, many genes and interactions between them likely contribute to individual differences in personality, behaviour and health. As social scientists often work with more than ten variables, determining the number of affected genes also poses methodological challenges. More collaboration between medical researchers, geneticists and social scientists has been advocated to increase knowledge in this field of study.

Some researchers note that pharmacological therapies may eventually be used to reverse epigenetic changes. Others caution that more research is necessary as drugs are known to modify the activity of multiple genes and may, therefore, cause serious side effects. However, the ultimate goal is to find patterns of epigenetic changes that can be targeted to treat mental illness, and reverse the effects of childhood stressors, for example. If such treatable patterns eventually become well-established, the inability to access brains in living humans to identify them poses an obstacle to pharmacological treatment.

Although some research has translated findings from animals to humans, others caution about the extrapolation of animal epigenetic studies to humans. Limited access to human brain tissue has posed the greatest challenge to conducting human research. Not yet knowing if epigenetic changes in the blood and (non-brain) tissues parallel modifications in the brain, places even greater reliance on brain research.

Much research is cross-sectional in that it establishes associations. More longitudinal research is necessary to help establish causation. Lack of resources has also limited the number of intergenerational studies. Therefore, advancing longitudinal and multigenerational, experience-dependent studies will be critical to further understanding the role of epigenetics in psychology.

See also

• Psychology
• Personality psychology
• Nature versus nurture
• Epigenetics
• Genetics
• Neuroscience
• Behavioral neuroscience
• Hypothalamic–pituitary–adrenal axis
• DNA
• Gene
• Cognition
• Mental health

Further reading

• Lester BM, Tronick E, Nestler E, Abel T, Kosofsky B, Kuzawa CW, Marsit CJ, Maze I, Meaney MJ, Monteggia LM, Reul JM, Skuse DH, Sweatt JD, Wood MA (2011). "Behavioral epigenetics". Ann. N. Y. Acad. Sci. 1226: 14–33. doi:10.1111/j.1749-6632.2011.06037.x. PMID 21615751. {{cite journal}}: Unknown parameter |month= ignored (help)CS1 maint: multiple names: authors list (link)
• Champagne FA, Rissman EF (2011). "Behavioral epigenetics: a new frontier in the study of hormones and behavior". Horm Behav. 59 (3): 277–8. doi:10.1016/j.yhbeh.2011.02.011. PMID 21419246. {{cite journal}}: Unknown parameter |month= ignored (help)
• Nelson ED, Monteggia LM (2011). "Epigenetics in the mature mammalian brain: effects on behavior and synaptic transmission". Neurobiol Learn Mem. 96 (1): 53–60. doi:10.1016/j.nlm.2011.02.015. PMID 21396474. {{cite journal}}: Unknown parameter |month= ignored (help)
• Plazas-Mayorca MD, Vrana KE (2011). "Proteomic investigation of epigenetics in neuropsychiatric disorders: a missing link between genetics and behavior?". J. Proteome Res. 10 (1): 58–65. doi:10.1021/pr100463y. PMC 3017635. PMID 20735116. {{cite journal}}: Unknown parameter |month= ignored (help)
• Curley JP, Jensen CL, Mashoodh R, Champagne FA (2011). "Social influences on neurobiology and behavior: epigenetic effects during development". Psychoneuroendocrinology. 36 (3): 352–71. doi:10.1016/j.psyneuen.2010.06.005. PMID 20650569. {{cite journal}}: Unknown parameter |month= ignored (help)CS1 maint: multiple names: authors list (link)
• Crews D (2011). "Epigenetic modifications of brain and behavior: theory and practice". Horm Behav. 59 (3): 393–8. doi:10.1016/j.yhbeh.2010.07.001. PMID 20633562. {{cite journal}}: Unknown parameter |month= ignored (help)
• Mann JJ, Currier DM (2010). "Stress, genetics and epigenetic effects on the neurobiology of suicidal behavior and depression". Eur. Psychiatry. 25 (5): 268–71. doi:10.1016/j.eurpsy.2010.01.009. PMC 2896004. PMID 20451357. {{cite journal}}: Unknown parameter |month= ignored (help)
• Crews D (2010). "Epigenetics, brain, behavior, and the environment". Hormones (Athens). 9 (1): 41–50. PMID 20363720.
• Malvaez M, Barrett RM, Wood MA, Sanchis-Segura C (2009). "Epigenetic mechanisms underlying extinction of memory and drug-seeking behavior". Mamm. Genome. 20 (9–10): 612–23. doi:10.1007/s00335-009-9224-3. PMC 3157916. PMID 19789849.{{cite journal}}: CS1 maint: multiple names: authors list (link)
• Nicolaïdis S (2008). "Prenatal imprinting of postnatal specific appetites and feeding behavior". Metab. Clin. Exp. 57 Suppl 2: S22–6. doi:10.1016/j.metabol.2008.07.004. PMID 18803961. {{cite journal}}: Unknown parameter |month= ignored (help)
• McGowan PO, Meaney MJ, Szyf M (2008). "Diet and the epigenetic (re)programming of phenotypic differences in behavior". Brain Res. 1237: 12–24. doi:10.1016/j.brainres.2008.07.074. PMC 2951010. PMID 18694740. {{cite journal}}: Unknown parameter |month= ignored (help)CS1 maint: multiple names: authors list (link)
• Szyf M, Weaver I, Meaney M (2007). "Maternal care, the epigenome and phenotypic differences in behavior". Reprod. Toxicol. 24 (1): 9–19. doi:10.1016/j.reprotox.2007.05.001. PMID 17561370. {{cite journal}}: Unknown parameter |month= ignored (help)CS1 maint: multiple names: authors list (link)
• Harmon K (2010-08-26). First Ant Genomes Promise Insight into Epigenetics and Longevity. Scientific American Magazine.

External links

• McDonald B (2011). "The Fingerprints of Poverty". Quirks & Quarks. CBC Radio. Audio interview with Dr. Moshe Szyf, a professor of Pharmacology and Therapeutics at McGill University, discusses how epigenetic changes are related to differences in socioeconomic status.
• Paylor B (2010). "Epigenetic Landscapes". This video addresses how, in principle, accumulated epigenetic changes may result in personality differences in identical twins. This science film was made by a Ph.D candidate in experimental medicine and award winning filmmaker Ben Paylor.
• Oz M (2011). "Control Your Pregnancy". The Dr. Oz Show. Video explaining how epigenetics can affect the unborn fetus.