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PMJ 90th anniversary review
Adaptation: a contemporary view, revisiting Crichton-Miller’s 1925 paper Graham Music Correspondence to Dr Graham Music, Portman Clinic, The Tavistock and Portman NHS Foundation Trust, 8 Fitzjohn’s Avenue, London NW3 5NA, UK; [email protected] Received 13 October 2015 Revised 29 December 2015 Accepted 18 January 2016
To cite: Music G. Postgrad Med J 2016;92:128–133. 128
ABSTRACT In this paper I discuss a contemporary ‘take’ on the concept of adaptation in light of Crichton-Miller’s original 1926 paper. I look briefly at some of the ways that contemporary thinking is both similar to and different from ideas of 90 years ago. In particular I think about how recent neurobiological findings, epigenetic research and attachment theory have cast new light on our understanding of the ways humans adapt to social and emotional environments. It looks at how psychiatric presentations which are seen as maladaptive might well have an adaptive origin in early life. In this account I emphasise how a more modern version of evolutionary theory can be developed, particularly one influenced by life history theory, and suggest that such ideas have powerful explanatory power as well as being based solidly in good research.
In 1925, Hugh Crichton-Miller wrote a seminal paper on adaptation which incorporated evolutionary ideas, psychology, endocrinology and psychoanalytic thinking. It is fascinating to consider how far we have come since then, but also how similar our preoccupations are. Crichton-Miller was a towering figure in his day, maybe best known as the founder of the Tavistock Clinic, where I also now work. His thinking at the time was at the cutting edge, and the Tavistock was seen as a centre of innovation and radicalism. I concentrate primarily on angles that I feel are important in relation to the extraordinary human capacity to adapt to environments. I ask how and why children and adults develop as they do, and try to think about the dangers of a short-sighted view of what we mean by a behaviour being viewed as pathological or not adaptive. Evolutionary thinking will feature centrally. I look at some current thinking about why certain traits and ways of behaving might survive and even thrive when these same behaviours might be seen as maladaptive. I also use attachment theory as a template for discussing what we mean by a successful adaptation and to consider whether a character trait might develop as an extremely successful adaptation to specific circumstances but not aid the carrier in other environments. Attachment theory of course was developed by John Bowlby at the Tavistock, and indeed is maybe the Tavistock’s main legacy. I will also look at the burgeoning science of epigenetics and think about the role of genes as opposed to environment, nature and nurture.1 Crichton-Miller had a view about characterological genetic inheritance which was influenced by Jung and others, and was current at the time but might now be viewed as dangerous, even racist. For
example he wrote about ‘the intellectual brilliance of the Jew, his facility in adaptation, notably economic … the stolidity of the Teuton, his incapacity to see beyond the objective’ and the ‘instability of the Latin’, not sentiments that would have much credence today. Nevertheless epigenetic research is challenging us to think again about Darwinian categories and the mechanisms whereby traits can be passed onto subsequent generations and why such processes might be adaptive. It also challenges us to rethink ideas about resilience and what we mean by this, and the risk of confusing resilience with adaptation.
DARWINIAN PSYCHOLOGY Humans are extraordinarily adaptive. We can survive in high altitudes, in Saharan heat, in Arctic ice, and we can also survive in a range of emotional climates. We are far more adaptive than any of our primate cousins, hence our success at colonising the world, albeit possibly at huge cost. By adaptive I mean finding ways of fitting into or managing to survive in the environment one finds oneself, and hence maximising the chances of reproducing. I am eschewing the slightly more moralistic definition Crichton-Miller uses. He described adaptation as how our inherited capacities respond to environmental influences while maintaining ‘internal harmony and social efficiency’, a statement which some might still agree with. Where I differ is on his view that ‘the neurotic, the insane, the delinquent constitute the three great groups of unsuccessful adaptations’. I suggest that at least the roots of most such behaviours might have begun as adaptive. In order to survive and reproduce humans need to have a range of potential strategies, as well as mechanisms whereby these strategies might be turned on or off. This is examined later, in particular the propensity to develop either a faster or slower life course. First though, maybe it pays to revisit basic Darwinian notions of survival. Darwin’s work has of course been misrepresented, such as in Spencer’s2 social Darwinism with its more worrying claims about survival of the fittest. In the worst case, this has led to ideas such as eugenics as well as, for example, poverty and lack of success being due to bad genes. However there are some basic Darwinist ideas that remain hugely pertinent. Darwin of course did not suggest that the ‘fittest’ survive, but rather that those with the best ‘fit’ do. So for example, take the question of why women might live well past child-rearing age, unlike in most species. Research evidence has shown that infants in many traditional, and even contemporary societies, are more
Music G. Postgrad Med J 2016;92:128–133. doi:10.1136/postgradmedj-2015-133708
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PMJ 90th anniversary review likely to survive if they have grandmothers on-hand. For example, in the Hadza, a hunter-gatherer group in Tanzania, having an alive and contributing grandmother enhanced survival rates in times of food shortages.3 Higher rates of survival of children, and shorter spaces between births, have been found in many societies where grandmaternal support is strong.4 One might assume then that the surviving babies might pass on traits linked to female longevity while the dying infants without alive grandmothers would not pass on their more short-lived traits. Similarly it seems likely that babies who cried and protested were more likely to survive in our evolutionary past, hence passing on that character trait as opposed to passive babies who might be left to die. Crying evolved for infants to communicate distress and is mostly biologically adaptive. Crying evokes different responses depending on cultural expectations and parental states of mind. Many adults prefer ‘good’ calm babies, but that is not always the case. In a period of bad drought in the 1970s some Maasai babies were labelled either ‘difficult’ or ‘easy’, based on how adaptable, calm or manageable they were.5 A researcher identified the 10 easiest and most difficult babies, but when he returned 3 months later the drought had worsened. He found 13 infants again and of these 7 already malnourished ones died in the coming months, but interestingly only 1 of the 7 was in the ‘difficult’ group. The fretful crying babies may have got more attention, or more milk, and showed more fight. In the study by Scheper-Hughes6 of Brazilian Shanty towns with high infant mortality rates, it was the babies labelled as ‘fighters’ who received the attention and they were the ones who lived, and hence had the best chance of passing on their ‘fighting’ character traits. Similarly infant survival is enhanced by actively attempting to elicit ‘bonding’ reactions in adults, and hence they are primed to relate to people and faces. Many of an infant’s earliest abilities are geared to becoming social beings, such as being drawn towards their mother’s voices7 and smells. Infants generally show preference for looking at faces over inanimate objects. In the first minutes of life their attention can be drawn to a black and white drawing of a face, but not to fuzzier, less distinct variants. Mothers and babies often seek out each other’s eyes after birth, and newborns prefer pictures of their own mother’s face to a stranger’s.8 By 3 months infants even prefer faces of their own race,9 presumably because fitting into the group (adapting), and recognising faces of safe others, enhances survival and evolutionary fitness. The logic behind these examples is that genetic traits that allow an organism to successfully adapt to its environment are likely to then be passed on. Some genes are more likely to survive in some environments than others. For example people suffering from attention deficit hyperactivity disorder (ADHD) are more likely to have a particular (long) version of the dopamine receptor gene.10 This seems to predispose to sensation seeking, even restlessness. Why might a trait survive that gives rise to such a poor prognosis as ADHD? It seems that such a temperament might well be selected for evolutionary reasons because it is advantageous in some environments. Examination of large samples of people involved in major migrations reveals that a higher proportion than average had the same ‘noveltyseeking’ genetic variant that leads to ADHD in children.11 One can speculate that for these people such novelty seeking might have aided those whose survival depended on finding new territories. To add yet another twist, about a seventh of a Kenyan tribe, the Ariaal, had this long version of the DRD4 gene. The Ariaal live either a nomadic life, moving from place to place, or a more settled pastoral life. Of those with the novelty-seeking Music G. Postgrad Med J 2016;92:128–133. doi:10.1136/postgradmedj-2015-133708
allele, those living a nomadic life, wondering across territories with sheep and goats, were well nourished and healthy, whereas those with this same allele living a settled pastoral life were less well nourished.12 It seems that having the ‘ADHD-inducing’ variant might well be a more adaptive option when living a less settled kind of life. There are countless other examples of a more traditional Darwinist take on why some traits survive and get passed on because they are adaptive. I now turn to look at how humans do not just inherit a genetic propensity but that we have a range of possible developmental trajectories, and these might be turned on or off because they are adaptive to a particular family, context, society or environment.
ATTACHMENT THEORY Attachment theory, developed at the Tavistock but about four decades later than Crichton-Miller’s paper, has shown how children develop emotional styles which are essentially adaptations to their parents’ psychological and interpersonal styles and beliefs. Young infants quickly learn their own cultural norms, including the emotional norms of their family, whether loving or violent or coldly callous, just as they can, for example, learn any language in the 1st year, even if such abilities soon fade.13 A test devised by Bowlby’s student Ainsworth14 looked at how infants respond when their mother leaves them briefly and when she returns. Some cry, scream and crawl towards the door but quickly calm on the mother’s return, others seem to barely notice their mothers leave, and still others are very preoccupied with their mothers before and after separations and cannot settle. Babies who came to be classified as securely attached were those who cry when their mother leaves, but who greet their mother’s return with relief, and sometimes delight, and then quickly settle back into a relaxed state. Another group, called avoidant, develop a deactivating strategy, seeming not to notice when their mothers leave, although in fact when left their physiological stress symptoms in fact increase similarly to securely attached children.15 In ambivalent attachment infants are preoccupied and clingy before their mother even left, and on her return they remained vigilant and unsettled, or hyperactivated. These responses make complete sense. The best chance of survival comes from working out how to behave in order to retain closeness to one’s attachment figures, whatever their emotional style. There is no point acting in an emotionally open and secure way if your parent will push you away as a result. So-called secure children, on the other hand, learn to trust that their feelings will be heard and listened to and that their caregivers will be there for them when needed. Thus for them it makes sense to become confident, outgoing, and interested in thoughts and feelings. Many children who have been traumatised might be seen as ‘naughty’, ‘bad’ or not adapting to social norms. However in reality these behaviours are often signs of humans’ malleable capacity to fit into any culture or group. We see more of what we call psychological ‘problems’ in children with insecure attachment styles and so can tend to assume that these styles are unhealthy or pathological, an assumption that runs counter to an evolutionary understanding. If you have parents who are inconsistent and chaotic, it makes no sense to be trusting, open and loving. Indeed being relaxed in the face of danger can put one’s very survival at risk. Children may thus become hyperattuned to their attachment figures, extremely sensitive to any hint of withdrawal, aggression or intrusion, and consequently become both needy and 129
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PMJ 90th anniversary review defensive in later relationships and struggle to relate empathically. Similarly if a child’s parents are neglectful, distant and unresponsive, or get cross or withdraw in the face of crying or other strong emotions, then it makes adaptive sense to develop a dampened down and avoidant attachment style which is more out of touch with one’s own and other people’s emotional states. Thus we can view most attachment strategies as successful adaptations to early contexts. In humans and most species the character traits that give the best chance of surviving and reproducing in harsh, unpredictable or dangerous environments are different from those that are successful in mild, stable and benign environments. Human developmental plasticity allows for survival in a range of emotional environments, from cruel to neglectful to kind. Of course when maltreated children come into a new environment, such as an adoptive family, they have already adapted to their early environment, and this early learning is hard to undo, and they thus can be responding to the adults in the current lives as if they were the same as previously traumatising adults.
Michael, 10, had been profoundly neglected and had received little attuned emotional input, and indeed had been left alone for much of his infancy. In response he had developed a dampened down, cut-off, almost dissociated way of being, barely able to recognise other people’s emotions, nor his own, and showing little interest in others and hardly any enthusiasm for life. This made him hard to relate and to warm to. Children like Michael are often labelled, maybe as ‘surly’ or ‘difficult’, leading to the adults becoming exasperated, critical and even rejecting. Michael needed help adapting to his new environment. Jim was different to Michael. He came from a violent home with unpredictable parents. He had a hypervigilant state of mind that had helped him survive in such a terrifying environment, becoming able to predict when aggression was about to erupt or when a parent had been drinking. Such adaptations led to an overawareness of others’ moods and states of mind, and oversensitivity to danger, criticism and any hint of not being accepted. It also made him prone to over-react and be highly distrustful and aggressive, leading him often to be labelled as ‘bad’ or ‘naughty’ or ‘impossible’ or worse. While early environments are not a life sentence they are nevertheless profoundly influential and their effects are more likely to remain in place without skilled input. Maltreated children may have adapted too successfully to their original traumatising world and struggle to readapt to, or even begin to believe in, an adult world that is better, safer, more kindly than the one they have come from.
ADAPTIVE BRAINS AND NERVOUS SYSTEMS We now know of course that the human brain is malleable and highly adaptive to its environment. We can think about the brain as like an extraordinarily complex muscle group, the parts that are used are strengthened from being exercised while others can wither from neglect.16 The human brain at birth has an overabundance of cells and in the postnatal period there is a process of pruning, sometimes referred to as ‘use it or lose it’, and cells that are not used simply die off. Schwartz and Begley ( p. 117)17 quote a figure of 20 billion synapses pruned every day between childhood and early adolescence, saying: ‘like bus 130
routes with no customers, they go out of business.’ Once a connection is formed it remains wired and new experience is filtered through already formed pathways, just as water will naturally flow down already formed channels, illustrating the idea that ‘cells that fire together wire together’.18 It is in this way that a child’s early context gives rise to particular beliefs and specific brain pathways which form at the expense of other potential pathways and become standard ways by which they experience the world. The human brain learns fast, and is an extraordinarily powerful predictor of the future. Early experiences become embodied in brain architecture, cells in our bodies, hormonal programming and posture as well as in psychological states and narratives about life. As Perry wrote,19 transitory states like fear can become traits, or in attachment patterns, momentary responses can become behavioural patterns and expectations of relationships. This all normally happens outside conscious awareness. A whole host of research is combining to show that trauma and abuse affect a range of brain areas.20 Those subjected to trauma and violence have higher activation of the amygdala, central to processing fear and other strong emotions, leading them to be more reactive and less still and calm,21 22 again presumably adaptive for scary environments. They tend to spot anger more quickly than other children, and emotionally reactive brain areas such as the amygdala are firing up more powerfully.23 In children adopted from highly neglectful as opposed to abusive backgrounds, on the other hand, there is less amygdala activation when witnessing anger or other high levels of emotion, which again was presumably adaptive for children who needed to turn away from an interest in other people’s thoughts and feelings to find a way to regulate their own emotions. Childhood trauma is also linked to less activation of prefrontal areas such as the ventromedial prefrontal cortex in children who have suffered maltreatment.24 These prefrontal areas are vital for capacities such as empathy and emotional regulation, and their deactivation accounts for some of the problems maltreated children have in managing ordinary life experiences that other children take in their stride. However, again when under threat, empathy and emotional regulation are far less useful than being very reactive. When in danger we tend to become highly aroused, and resort to primitive survival responses such as fight or flight, or even freeze. Our whole being and physiology then is geared to coming through the threat, as we tense up and prepare for trouble, while other bodily functions, such as digestion or immune responses, temporarily go into abeyance, as do higher order thought processes. People who have suffered extreme trauma can go into such states very quickly. Porges25 has taken such an evolutionary view a step further in relation to our autonomic nervous systems. He shows that we have three very different kinds of autonomic responses each rooted in a different stage of our phylogenetic history. Our most primitive reaction, based on the evolutionarily ancient dorsal vagus nerve, is one we share with the least developed of vertebrates and its activation leads to complete immobilisation, freezing and the closing down of our systems. Dissociation and metabolic shutdown are typical of this extreme ‘rabbit in headlights’ system. It is adaptive because predators are not attracted to creatures that seem lifeless. Many traumatised and neglected children and adults can present like this. An evolutionarily more advanced response, present in mammals, is seen when our sympathetic nervous system fires up, for example in fight-flight responses. This system’s responses include increased heart rate, sweating, and quicker breathing, Music G. Postgrad Med J 2016;92:128–133. doi:10.1136/postgradmedj-2015-133708
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PMJ 90th anniversary review dilation of the eyes, feeling cold and inhibited digestion. It goes into action when we feel anxiety or terror, and when attachment anxieties are triggered. We need this arousal system and all experience times when we resort to it, but those in a violent environment, for example, will have a much more highly activated sympathetic nervous system. In other words they will be easily aroused, and find it hard to calm down, concentrate or feel at ease, reactions which are not adaptive for school or work life or good friendships. While we are designed to resort to sympathetic arousal states when danger looms, we are also designed to calm down quickly afterwards. However chronic bad experiences can lead to people being stuck in anxious fearful states. The evolutionarily most advanced aspect of our autonomic nervous systems is seen in the action of our ventral (smart) vagus, which links heart, gut, brainstem and other viscera and is active when we feel calm, at ease and safe. Its activation is linked to an activated social engagement system, to feeling good and secure, and to many positive health outcomes. Again though, it is adaptive for it to turn off in the face of threat, as feeling ‘chilled’ is unhelpful in the face of danger. Even our hormones are affected by our contexts, environments and experiences. One study found that boys brought up in areas with more boarded-up buildings had higher testosterone levels, and were more risk-taking than boys from similar social groups living in less run down neighbourhoods.26 Higher testosterone is linked with increased aggression, and it makes sense that one might non-consciously become more risk-taking and aggressive when the context feels unsafe. Similarly in deprived environments, just having access to more green space is linked to healthier cortisol levels.27 Thus hormonal levels are not a given, but are affected by experiences. If we have many good early experiences we will release more oxytocin,28 while stressful or abusive childhoods lead to lower baseline levels of oxytocin.29 We will also develop more oxytocin receptors in our bodies. The same is true of the stress hormone cortisol,30 with high levels in stressed or depressed people or extremely low levels in post-traumatic stress disorder (PTSD).31 In terms of serotonin we of course see low levels of it in depression32 and after bad experiences.33 Dopamine, central to the reward system and activated when we are positive, excited or eager, is another hormone that is profoundly affected by early experiences. Depressed mothers have low dopamine levels, and so do their babies as young as a month old. Thus not just our mental states but our brains and bodies adapt profoundly to our psychological context.
GENES, ENVIRONMENT, EPIGENETICS An important twist has been added to the adaptation story by the growing science of epigenetics which has shown how genes can either be expressed or silenced in response to particular kinds of experiences, via methylation (or demethylation) processes. Interestingly even brief stressful experiences in adults, such as a 90 min mock stressful job interview including difficult arithmetical questions, was shown to alter the action of a gene central to oxytocin production.34 Adverse early experiences have a more powerful effect on how genes are expressed.35 For example recent studies36 demonstrated that stress or trauma was correlated with higher methylation of a gene, exon 1F of NR3C1. More hopefully psychotherapy has been shown to positively affect gene expression, for example reducing the extent of methylation of the BDNF genes in adults who suffered childhood trauma.37 Experiences such as of trauma do not change the genes we inherit but they leave their mark, and indeed it seems that this Music G. Postgrad Med J 2016;92:128–133. doi:10.1136/postgradmedj-2015-133708
mark can transfer across generations, affecting how genes get expressed down the line.38 This has, for example, been seen in mice exposed to fearful experiences. When pups of these mice were exposed to the same stressor they showed fear, and the process whereby this occurred is DNA methylation.39 Holocaust survivors similarly seem to pass aspects of their stress response to their children via such processes.40 This again is adaptive, even if it smacks more of Lamarck41 than Darwin. If you live in a world where you expect trauma then you are more likely to survive if you are prepared, and in this case this survival and adaptation is enhanced by epigenetic mechanisms. What also is of interest is that some of us are more adaptable than others, or in other words some of us are less influenced by either good or bad experiences. This is called the ‘differential susceptibility to rearing hypothesis’.42 For example, if one has one of two versions of a dopamine receptor gene and has adverse early experiences then one’s outcomes (eg, mental health problems or increased risk taking) are likely to be worse.43 Similarly we can have one of two versions of the 5HT serotonin receptor gene, and those with the short version are more vulnerable to trauma and neglect,44 in the face of bad experiences being more prone to aggression, anxiety and depression. Such responsive and more easily influenced children are sometimes called ‘orchids’ as opposed to ‘dandelions’, as they grew particularly well only in special soil and do poorly in bad environments while the ‘dandelions’ grow anywhere. The orchids also benefit more from positive inputs such as therapeutic interventions.45 Thus some people are, for genetic reasons, more likely to be affected by both good and bad experiences.46 This raises interesting questions. The orchids may be more adaptive, which in some situations makes them more resilient and in others, less so.
LIFE HISTORY ADAPTATIONS We are all the time adapting to our environments, and this triggers neurobiological patterns that have a profound effect.47 Those born into highly stressed worlds tend to have a speeded up metabolism, faster heart rates, more activated stress response systems and develop, what some call, a fast as opposed to a slow life course strategy. We see this in a range of other mammals as well as humans, and it is a strategy that aids survival. We all have this in our evolutionary back-pocket, as otherwise any too trusting and complacent ancestors might well have met a violent end before they had time to reproduce. In some circumstances the best response is to be wary, vigilant and untrusting. Life history programming is so powerful that girls with insecure attachments tend to reach puberty earlier,48 as do those born into highly stressed families, or adopted from poor quality orphanages, or without fathers, and they are more likely to get involved in sexual activity younger, and reproduce earlier and more often.49 There is an evolutionary explanation for this which can only be speculative but which I think is plausible. In a dangerous world those who wait too long to reproduce might not survive long enough to do so, so starting early might aid passing on one’s genes.50 Perhaps this is why animals, including humans, tend to take more risks when their environments are unstable, becoming more involved in violence or promiscuity for example, and living a more highly stressed life. Research based on life history theory, propounded by many evolutionary psychologists,51 seems to be showing that if we are born into an environment where stress, anxiety, fear or trauma are likely, then we live a ‘faster life course’, and for example, breed earlier,48 take more risks and also die younger and have worse health along the way. Children with secure attachment 131
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PMJ 90th anniversary review styles, living in safe, relaxed environments, will non-consciously pick up very different messages, such as that it is sensible to wait longer to reproduce, it is safe to relax and trust the world, it is fine to have less children but to invest more in each one, and that one can rely on long-term stable relationships. When people are given cues that suggest a dangerous situation, those brought up in poorer socioeconomic circumstances tend to take more risks, while those brought up economically advantaged tend to take the slower, more risk-averse strategy.52 Unfortunately, while these neurobiological responses might be adaptive in that they aid survival, they have worrying longerterm sequelae. The classic study is a longitudinal one of over 17 000 people, called ACE, which measures averse childhood experiences,53 and people with the most adverse early experiences, such as of trauma, abuse or loss, end up suffering the worse health as they age, and indeed tend to die younger, often from diseases linked to metabolic syndrome.54 Such diseases, such as heart attacks, strokes and diabetes, are very linked with our stress responses. Thus a burgeoning body of research shows how exposure early on to stress has a profound physical effect, altering immune functioning, increasing the risk of all manner of diseases later on in life, including cancers. One study55 linked adverse experiences with issues ranging from increased smoking, alcohol and drug use, obesity and suicidality, all of which increased with more adverse experiences. Compared with persons with an ACE score of 0, those with an ACE score of 4 or more were twice as likely to be smokers, 12 times more likely to have attempted suicide, 7 times more likely to be alcoholic and 10 times more likely to have injected street drugs. A highly stressed life is also linked with a central telltale sign of physical ill-health and risk of early death, shorter telomeres.56 There appears to be a dose related response, so that the more the stress, the bigger effect on telomere length and the more likelihood of all kinds of diseases, from cancer to diabetes to heart disease.57 Indeed a recent study even found that stress in intrauterine life gave rise to shortened telomeres right up until adulthood.58 While at first glance such responses might seem maladaptive, what we see here is a tension between different options. A fast life course might be viewed as a kind of trade-off, sacrificing good health and longevity for immediate survival and a better chance of reproducing.59 This is an adaptive response, enhancing the passing on of genes successfully simply by increasing the chances of survival, but it is also a strategy that has lasting ill effects on psychological and physiological well-being.51
CONCLUSION The current story about adaptation has similar preoccupations to Crichton-Miller’s 1926 one in terms of working out how our nature adapts to our nurture.1 What has changed maybe, is our newer understanding of why certain seemingly maladaptive patterns might exist for good evolutionary and biological reasons. When Crichton-Miller suggests that the murderer is like the ‘infant of the human race’, and that many mentally ill are stuck in primitive functioning, his language may jar but perhaps in some ways his views are not so far away from contemporary ones. When under massive stress or feeling fearful we do, for example, rely on evolutionarily earlier aspects of our brains (eg, less prefrontal activation) and of our nervous systems (less reliance on ventral vagus system). Hypervigilance and alertness to potential danger would aid the chances of survival in frightening and uncertain environments. Similarly being emotionally cut-off helps survive in families where feelings are seen as bad. In tough, ruthless situations, 132
it does not pay to be kind and trusting, whereas being aggressive, selfish and ruthless might be more successful. Maybe what has changed since Crichton-Miller’s days is that we have begun to take the judgement out of our analysis and to take a more compassionate stance towards suffering and what some still see as maladaptation. While we live in a political climate in which criminality, the mentally unstable and even the poor are blamed for their plight, evolutionary theory is increasingly making sense of why such patterns might have adaptive origins. This should encourage us to argue for the conditions which would facilitate more health-inducing adaptations, such as those seen in securely attached, less stressed and more confident people.
Main messages ▸ Humans are highly adaptive, maybe more so than most species, and this extends to emotional adaptation. ▸ Behaviours that are adaptive in one context can become maladaptive in others. ▸ Adaptation occurs via the usual Darwinian selection processes. ▸ We also adapt due to having a range of potential pathways which can be turned on or off. ▸ Experiences affect our trajectory right down to a cellular level.
Current research questions ▸ Can early patterns be shifted, especially after trauma? ▸ What epigenetic effects might we see from positive experiences (such as therapy or adoption)? ▸ What responses to environmental impingements might start as adaptive and which might not? ▸ At what level ( psychological, bodily treatments, drugs, etc) might we make the most effective interventions?
Key references ▸ Hrdy SB. Mother Nature: Natural Selection and the Female of the Species. London: Chatto & Windus, 1999. ▸ Bowlby J. Attachment and loss. Volume 1 Attachment. London: Hogarth, 1969. ▸ McCrory E, De Brito SA, Viding E. Research review: the neurobiology and genetics of maltreatment and adversity. J Child Psychol Psychiatry 2010;51:1079–95. ▸ Music G. The Good Life: Wellbeing and the new science of altruism, selfishness and immorality. London: Routledge, 2014. ▸ Moule RK, Decker SH, Pyrooz DC. Social Capital, the Life-Course, and Gangs. Handb Life-Course Criminol 2013:143–58. Twitter Follow Graham Music at @grahammusic1 Competing interests None declared. Provenance and peer review Commissioned; externally peer reviewed. Music G. Postgrad Med J 2016;92:128–133. doi:10.1136/postgradmedj-2015-133708
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Music G. Nurturing natures: attachment and children’s emotional, social and brain development. London: Psychology Press, 2010. Spencer H. The principles of sociology. vol. 6. New York: Appleton, 1895. Hawkes K, Coxworth JE. Grandmothers and the evolution of human longevity: a review of findings and future directions. Evol Anthropol Issues News Rev 2013;22:294–302. Kramer KL, Otárola-Castillo E. When mothers need others: The impact of hominin life history evolution on cooperative breeding. J Hum Evol 2015;84:16–24. Wermke K, Friederici AD. Developmental changes of infant cries–the evolution of complex vocalizations. Behav Brain Sci 2005;27:474–5. Scheper-Hughes N. Death without weeping: the violence of everyday life in Brazil. California: University of California Press, 1992. DeCasper AJ, Fifer WP. Of human bonding: newborns prefer their mothers’ voices. Science 1980;208:1174. Wagner JB, Luyster RJ, Yim JY, et al. The role of early visual attention in social development. Int J Behav Dev 2013;37:118–124. Gaither SE, Pauker K, Johnson SP. Biracial and monoracial infant own-race face perception: an eye tracking study. Dev Sci 2012;15:775–82. Faraone SV, Doyle AE, Mick E, et al. Meta-analysis of the association between the 7-repeat allele of the dopamine D(4) receptor gene and attention deficit hyperactivity disorder. Am J Psychiatry 2001;158:1052–7. Chen C, Burton M, Greenberger E, et al. Population migration and the variation of dopamine D4 receptor (DRD4) allele frequencies around the globe. Evol Hum Behav 1999;20:309–24. Eisenberg DTA, Campbell B, Gray PB, et al. Dopamine receptor genetic polymorphisms and body composition in undernourished pastoralists: an exploration of nutrition indices among nomadic and recently settled Ariaal men of northern Kenya. BMC Evol Biol 2008;8:173. Kuhl PK, Stevens E, Hayashi A, et al. Infants show a facilitation effect for native language phonetic perception between 6 and 12 months. Dev Sci 2006;9:F13–F21. Ainsworth MDS. Patterns of attachment: a psychological study of the strange situation. New Jersey: Lawrence Erlbaum, 1978. Sroufe LA, Waters E. Attachment as an organizational construct. Child Dev 1977;48:1184–99. Music G. Neglecting neglect: some thoughts about children who have lacked good input, and are ‘undrawn’ and ‘unenjoyed’. J Child Psychol 2009;35:142–56. Schwartz J, Begley S. The mind and the brain: neuroplasticity and the power of mental force. New York: Harper, 2002. Hebb DO. The organisation of behaviour. New York: Wiley, 1949. Perry BD, Pollard RA, Blakley TL, et al. Childhood trauma, the neurobiology of adaptation, and Use-dependent development of the brain: how states become traits, Infant Ment. Health J 1995;16:271–91. Teicher MH, Anderson CM, Polcari A. Childhood maltreatment is associated with reduced volume in the hippocampal subfields CA3, dentate gyrus, and subiculum. Proc Natl Acad Sci USA 2012;109:E563–72. Thomas KM, Drevets WC, Dahl RE, et al. Amygdala response to fearful faces in anxious and depressed children. Arch Gen Psychiatry 2001;58:1057–63. Sigurdsson T, Doyère V, Cain CK, et al. Long-term potentiation in the amygdala: a cellular mechanism of fear learning and memory. Neuropharmacology 2007;52:215–27. McCrory E, De Brito SA, Viding E. Research review: the neurobiology and genetics of maltreatment and adversity. J Child Psychol Psychiatry 2010;51:1079–95. Mehta MA, Golembo NI, Nosarti C, et al. Amygdala, hippocampal and corpus callosum size following severe early institutional deprivation: the English and Romanian Adoptees study pilot. J Child Psychol Psychiatry 2009;50:943–51. Porges SW. The polyvagal theory: neurophysiological foundations of emotions, attachment, communication, and self-regulation. New York: Norton, 2011. Tarter RE, Kirisci L, Gavaler JS, et al. Prospective study of the association between abandoned dwellings and testosterone level on the development of behaviors leading to cannabis use disorder in boys. Biol Psychiatry 2009;65:116–21. Roe JJ, Thompson CW, Aspinall PA, et al. Green space and stress: evidence from cortisol measures in deprived urban communities. Int J Environ Res Public Health 2013;10:4086–103. Zak PJ. The moral molecule: the new science of what makes us good or evil. London: Bantam Press, 2012. Bhandari R, Bakermans-Kranenburg MJ, van der Veen R, et al. Salivary oxytocin mediates the association between emotional maltreatment and responses to emotional infant faces. Physiol Behav 2014;131:123–8. Gerhardt S. Why love matters: how affection shapes a baby’s brain. Oxford: Routledge, 2014. Yehuda R. Biology of posttraumatic stress disorder. J Clin Psychiatry Suppl 2001;62:41–6.
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Adaptation: a contemporary view, revisiting Crichton-Miller's 1925 paper Graham Music Postgrad Med J 2016 92: 128-133 originally published online February 23, 2016
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PMJ 90th anniversary review
Adaptation: a contemporary view, revisiting Crichton-Miller’s 1925 paper Graham Music Correspondence to Dr Graham Music, Portman Clinic, The Tavistock and Portman NHS Foundation Trust, 8 Fitzjohn’s Avenue, London NW3 5NA, UK; [email protected] Received 13 October 2015 Revised 29 December 2015 Accepted 18 January 2016
To cite: Music G. Postgrad Med J 2016;92:128–133. 128
ABSTRACT In this paper I discuss a contemporary ‘take’ on the concept of adaptation in light of Crichton-Miller’s original 1926 paper. I look briefly at some of the ways that contemporary thinking is both similar to and different from ideas of 90 years ago. In particular I think about how recent neurobiological findings, epigenetic research and attachment theory have cast new light on our understanding of the ways humans adapt to social and emotional environments. It looks at how psychiatric presentations which are seen as maladaptive might well have an adaptive origin in early life. In this account I emphasise how a more modern version of evolutionary theory can be developed, particularly one influenced by life history theory, and suggest that such ideas have powerful explanatory power as well as being based solidly in good research.
In 1925, Hugh Crichton-Miller wrote a seminal paper on adaptation which incorporated evolutionary ideas, psychology, endocrinology and psychoanalytic thinking. It is fascinating to consider how far we have come since then, but also how similar our preoccupations are. Crichton-Miller was a towering figure in his day, maybe best known as the founder of the Tavistock Clinic, where I also now work. His thinking at the time was at the cutting edge, and the Tavistock was seen as a centre of innovation and radicalism. I concentrate primarily on angles that I feel are important in relation to the extraordinary human capacity to adapt to environments. I ask how and why children and adults develop as they do, and try to think about the dangers of a short-sighted view of what we mean by a behaviour being viewed as pathological or not adaptive. Evolutionary thinking will feature centrally. I look at some current thinking about why certain traits and ways of behaving might survive and even thrive when these same behaviours might be seen as maladaptive. I also use attachment theory as a template for discussing what we mean by a successful adaptation and to consider whether a character trait might develop as an extremely successful adaptation to specific circumstances but not aid the carrier in other environments. Attachment theory of course was developed by John Bowlby at the Tavistock, and indeed is maybe the Tavistock’s main legacy. I will also look at the burgeoning science of epigenetics and think about the role of genes as opposed to environment, nature and nurture.1 Crichton-Miller had a view about characterological genetic inheritance which was influenced by Jung and others, and was current at the time but might now be viewed as dangerous, even racist. For
example he wrote about ‘the intellectual brilliance of the Jew, his facility in adaptation, notably economic … the stolidity of the Teuton, his incapacity to see beyond the objective’ and the ‘instability of the Latin’, not sentiments that would have much credence today. Nevertheless epigenetic research is challenging us to think again about Darwinian categories and the mechanisms whereby traits can be passed onto subsequent generations and why such processes might be adaptive. It also challenges us to rethink ideas about resilience and what we mean by this, and the risk of confusing resilience with adaptation.
DARWINIAN PSYCHOLOGY Humans are extraordinarily adaptive. We can survive in high altitudes, in Saharan heat, in Arctic ice, and we can also survive in a range of emotional climates. We are far more adaptive than any of our primate cousins, hence our success at colonising the world, albeit possibly at huge cost. By adaptive I mean finding ways of fitting into or managing to survive in the environment one finds oneself, and hence maximising the chances of reproducing. I am eschewing the slightly more moralistic definition Crichton-Miller uses. He described adaptation as how our inherited capacities respond to environmental influences while maintaining ‘internal harmony and social efficiency’, a statement which some might still agree with. Where I differ is on his view that ‘the neurotic, the insane, the delinquent constitute the three great groups of unsuccessful adaptations’. I suggest that at least the roots of most such behaviours might have begun as adaptive. In order to survive and reproduce humans need to have a range of potential strategies, as well as mechanisms whereby these strategies might be turned on or off. This is examined later, in particular the propensity to develop either a faster or slower life course. First though, maybe it pays to revisit basic Darwinian notions of survival. Darwin’s work has of course been misrepresented, such as in Spencer’s2 social Darwinism with its more worrying claims about survival of the fittest. In the worst case, this has led to ideas such as eugenics as well as, for example, poverty and lack of success being due to bad genes. However there are some basic Darwinist ideas that remain hugely pertinent. Darwin of course did not suggest that the ‘fittest’ survive, but rather that those with the best ‘fit’ do. So for example, take the question of why women might live well past child-rearing age, unlike in most species. Research evidence has shown that infants in many traditional, and even contemporary societies, are more
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PMJ 90th anniversary review likely to survive if they have grandmothers on-hand. For example, in the Hadza, a hunter-gatherer group in Tanzania, having an alive and contributing grandmother enhanced survival rates in times of food shortages.3 Higher rates of survival of children, and shorter spaces between births, have been found in many societies where grandmaternal support is strong.4 One might assume then that the surviving babies might pass on traits linked to female longevity while the dying infants without alive grandmothers would not pass on their more short-lived traits. Similarly it seems likely that babies who cried and protested were more likely to survive in our evolutionary past, hence passing on that character trait as opposed to passive babies who might be left to die. Crying evolved for infants to communicate distress and is mostly biologically adaptive. Crying evokes different responses depending on cultural expectations and parental states of mind. Many adults prefer ‘good’ calm babies, but that is not always the case. In a period of bad drought in the 1970s some Maasai babies were labelled either ‘difficult’ or ‘easy’, based on how adaptable, calm or manageable they were.5 A researcher identified the 10 easiest and most difficult babies, but when he returned 3 months later the drought had worsened. He found 13 infants again and of these 7 already malnourished ones died in the coming months, but interestingly only 1 of the 7 was in the ‘difficult’ group. The fretful crying babies may have got more attention, or more milk, and showed more fight. In the study by Scheper-Hughes6 of Brazilian Shanty towns with high infant mortality rates, it was the babies labelled as ‘fighters’ who received the attention and they were the ones who lived, and hence had the best chance of passing on their ‘fighting’ character traits. Similarly infant survival is enhanced by actively attempting to elicit ‘bonding’ reactions in adults, and hence they are primed to relate to people and faces. Many of an infant’s earliest abilities are geared to becoming social beings, such as being drawn towards their mother’s voices7 and smells. Infants generally show preference for looking at faces over inanimate objects. In the first minutes of life their attention can be drawn to a black and white drawing of a face, but not to fuzzier, less distinct variants. Mothers and babies often seek out each other’s eyes after birth, and newborns prefer pictures of their own mother’s face to a stranger’s.8 By 3 months infants even prefer faces of their own race,9 presumably because fitting into the group (adapting), and recognising faces of safe others, enhances survival and evolutionary fitness. The logic behind these examples is that genetic traits that allow an organism to successfully adapt to its environment are likely to then be passed on. Some genes are more likely to survive in some environments than others. For example people suffering from attention deficit hyperactivity disorder (ADHD) are more likely to have a particular (long) version of the dopamine receptor gene.10 This seems to predispose to sensation seeking, even restlessness. Why might a trait survive that gives rise to such a poor prognosis as ADHD? It seems that such a temperament might well be selected for evolutionary reasons because it is advantageous in some environments. Examination of large samples of people involved in major migrations reveals that a higher proportion than average had the same ‘noveltyseeking’ genetic variant that leads to ADHD in children.11 One can speculate that for these people such novelty seeking might have aided those whose survival depended on finding new territories. To add yet another twist, about a seventh of a Kenyan tribe, the Ariaal, had this long version of the DRD4 gene. The Ariaal live either a nomadic life, moving from place to place, or a more settled pastoral life. Of those with the novelty-seeking Music G. Postgrad Med J 2016;92:128–133. doi:10.1136/postgradmedj-2015-133708
allele, those living a nomadic life, wondering across territories with sheep and goats, were well nourished and healthy, whereas those with this same allele living a settled pastoral life were less well nourished.12 It seems that having the ‘ADHD-inducing’ variant might well be a more adaptive option when living a less settled kind of life. There are countless other examples of a more traditional Darwinist take on why some traits survive and get passed on because they are adaptive. I now turn to look at how humans do not just inherit a genetic propensity but that we have a range of possible developmental trajectories, and these might be turned on or off because they are adaptive to a particular family, context, society or environment.
ATTACHMENT THEORY Attachment theory, developed at the Tavistock but about four decades later than Crichton-Miller’s paper, has shown how children develop emotional styles which are essentially adaptations to their parents’ psychological and interpersonal styles and beliefs. Young infants quickly learn their own cultural norms, including the emotional norms of their family, whether loving or violent or coldly callous, just as they can, for example, learn any language in the 1st year, even if such abilities soon fade.13 A test devised by Bowlby’s student Ainsworth14 looked at how infants respond when their mother leaves them briefly and when she returns. Some cry, scream and crawl towards the door but quickly calm on the mother’s return, others seem to barely notice their mothers leave, and still others are very preoccupied with their mothers before and after separations and cannot settle. Babies who came to be classified as securely attached were those who cry when their mother leaves, but who greet their mother’s return with relief, and sometimes delight, and then quickly settle back into a relaxed state. Another group, called avoidant, develop a deactivating strategy, seeming not to notice when their mothers leave, although in fact when left their physiological stress symptoms in fact increase similarly to securely attached children.15 In ambivalent attachment infants are preoccupied and clingy before their mother even left, and on her return they remained vigilant and unsettled, or hyperactivated. These responses make complete sense. The best chance of survival comes from working out how to behave in order to retain closeness to one’s attachment figures, whatever their emotional style. There is no point acting in an emotionally open and secure way if your parent will push you away as a result. So-called secure children, on the other hand, learn to trust that their feelings will be heard and listened to and that their caregivers will be there for them when needed. Thus for them it makes sense to become confident, outgoing, and interested in thoughts and feelings. Many children who have been traumatised might be seen as ‘naughty’, ‘bad’ or not adapting to social norms. However in reality these behaviours are often signs of humans’ malleable capacity to fit into any culture or group. We see more of what we call psychological ‘problems’ in children with insecure attachment styles and so can tend to assume that these styles are unhealthy or pathological, an assumption that runs counter to an evolutionary understanding. If you have parents who are inconsistent and chaotic, it makes no sense to be trusting, open and loving. Indeed being relaxed in the face of danger can put one’s very survival at risk. Children may thus become hyperattuned to their attachment figures, extremely sensitive to any hint of withdrawal, aggression or intrusion, and consequently become both needy and 129
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PMJ 90th anniversary review defensive in later relationships and struggle to relate empathically. Similarly if a child’s parents are neglectful, distant and unresponsive, or get cross or withdraw in the face of crying or other strong emotions, then it makes adaptive sense to develop a dampened down and avoidant attachment style which is more out of touch with one’s own and other people’s emotional states. Thus we can view most attachment strategies as successful adaptations to early contexts. In humans and most species the character traits that give the best chance of surviving and reproducing in harsh, unpredictable or dangerous environments are different from those that are successful in mild, stable and benign environments. Human developmental plasticity allows for survival in a range of emotional environments, from cruel to neglectful to kind. Of course when maltreated children come into a new environment, such as an adoptive family, they have already adapted to their early environment, and this early learning is hard to undo, and they thus can be responding to the adults in the current lives as if they were the same as previously traumatising adults.
Michael, 10, had been profoundly neglected and had received little attuned emotional input, and indeed had been left alone for much of his infancy. In response he had developed a dampened down, cut-off, almost dissociated way of being, barely able to recognise other people’s emotions, nor his own, and showing little interest in others and hardly any enthusiasm for life. This made him hard to relate and to warm to. Children like Michael are often labelled, maybe as ‘surly’ or ‘difficult’, leading to the adults becoming exasperated, critical and even rejecting. Michael needed help adapting to his new environment. Jim was different to Michael. He came from a violent home with unpredictable parents. He had a hypervigilant state of mind that had helped him survive in such a terrifying environment, becoming able to predict when aggression was about to erupt or when a parent had been drinking. Such adaptations led to an overawareness of others’ moods and states of mind, and oversensitivity to danger, criticism and any hint of not being accepted. It also made him prone to over-react and be highly distrustful and aggressive, leading him often to be labelled as ‘bad’ or ‘naughty’ or ‘impossible’ or worse. While early environments are not a life sentence they are nevertheless profoundly influential and their effects are more likely to remain in place without skilled input. Maltreated children may have adapted too successfully to their original traumatising world and struggle to readapt to, or even begin to believe in, an adult world that is better, safer, more kindly than the one they have come from.
ADAPTIVE BRAINS AND NERVOUS SYSTEMS We now know of course that the human brain is malleable and highly adaptive to its environment. We can think about the brain as like an extraordinarily complex muscle group, the parts that are used are strengthened from being exercised while others can wither from neglect.16 The human brain at birth has an overabundance of cells and in the postnatal period there is a process of pruning, sometimes referred to as ‘use it or lose it’, and cells that are not used simply die off. Schwartz and Begley ( p. 117)17 quote a figure of 20 billion synapses pruned every day between childhood and early adolescence, saying: ‘like bus 130
routes with no customers, they go out of business.’ Once a connection is formed it remains wired and new experience is filtered through already formed pathways, just as water will naturally flow down already formed channels, illustrating the idea that ‘cells that fire together wire together’.18 It is in this way that a child’s early context gives rise to particular beliefs and specific brain pathways which form at the expense of other potential pathways and become standard ways by which they experience the world. The human brain learns fast, and is an extraordinarily powerful predictor of the future. Early experiences become embodied in brain architecture, cells in our bodies, hormonal programming and posture as well as in psychological states and narratives about life. As Perry wrote,19 transitory states like fear can become traits, or in attachment patterns, momentary responses can become behavioural patterns and expectations of relationships. This all normally happens outside conscious awareness. A whole host of research is combining to show that trauma and abuse affect a range of brain areas.20 Those subjected to trauma and violence have higher activation of the amygdala, central to processing fear and other strong emotions, leading them to be more reactive and less still and calm,21 22 again presumably adaptive for scary environments. They tend to spot anger more quickly than other children, and emotionally reactive brain areas such as the amygdala are firing up more powerfully.23 In children adopted from highly neglectful as opposed to abusive backgrounds, on the other hand, there is less amygdala activation when witnessing anger or other high levels of emotion, which again was presumably adaptive for children who needed to turn away from an interest in other people’s thoughts and feelings to find a way to regulate their own emotions. Childhood trauma is also linked to less activation of prefrontal areas such as the ventromedial prefrontal cortex in children who have suffered maltreatment.24 These prefrontal areas are vital for capacities such as empathy and emotional regulation, and their deactivation accounts for some of the problems maltreated children have in managing ordinary life experiences that other children take in their stride. However, again when under threat, empathy and emotional regulation are far less useful than being very reactive. When in danger we tend to become highly aroused, and resort to primitive survival responses such as fight or flight, or even freeze. Our whole being and physiology then is geared to coming through the threat, as we tense up and prepare for trouble, while other bodily functions, such as digestion or immune responses, temporarily go into abeyance, as do higher order thought processes. People who have suffered extreme trauma can go into such states very quickly. Porges25 has taken such an evolutionary view a step further in relation to our autonomic nervous systems. He shows that we have three very different kinds of autonomic responses each rooted in a different stage of our phylogenetic history. Our most primitive reaction, based on the evolutionarily ancient dorsal vagus nerve, is one we share with the least developed of vertebrates and its activation leads to complete immobilisation, freezing and the closing down of our systems. Dissociation and metabolic shutdown are typical of this extreme ‘rabbit in headlights’ system. It is adaptive because predators are not attracted to creatures that seem lifeless. Many traumatised and neglected children and adults can present like this. An evolutionarily more advanced response, present in mammals, is seen when our sympathetic nervous system fires up, for example in fight-flight responses. This system’s responses include increased heart rate, sweating, and quicker breathing, Music G. Postgrad Med J 2016;92:128–133. doi:10.1136/postgradmedj-2015-133708
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PMJ 90th anniversary review dilation of the eyes, feeling cold and inhibited digestion. It goes into action when we feel anxiety or terror, and when attachment anxieties are triggered. We need this arousal system and all experience times when we resort to it, but those in a violent environment, for example, will have a much more highly activated sympathetic nervous system. In other words they will be easily aroused, and find it hard to calm down, concentrate or feel at ease, reactions which are not adaptive for school or work life or good friendships. While we are designed to resort to sympathetic arousal states when danger looms, we are also designed to calm down quickly afterwards. However chronic bad experiences can lead to people being stuck in anxious fearful states. The evolutionarily most advanced aspect of our autonomic nervous systems is seen in the action of our ventral (smart) vagus, which links heart, gut, brainstem and other viscera and is active when we feel calm, at ease and safe. Its activation is linked to an activated social engagement system, to feeling good and secure, and to many positive health outcomes. Again though, it is adaptive for it to turn off in the face of threat, as feeling ‘chilled’ is unhelpful in the face of danger. Even our hormones are affected by our contexts, environments and experiences. One study found that boys brought up in areas with more boarded-up buildings had higher testosterone levels, and were more risk-taking than boys from similar social groups living in less run down neighbourhoods.26 Higher testosterone is linked with increased aggression, and it makes sense that one might non-consciously become more risk-taking and aggressive when the context feels unsafe. Similarly in deprived environments, just having access to more green space is linked to healthier cortisol levels.27 Thus hormonal levels are not a given, but are affected by experiences. If we have many good early experiences we will release more oxytocin,28 while stressful or abusive childhoods lead to lower baseline levels of oxytocin.29 We will also develop more oxytocin receptors in our bodies. The same is true of the stress hormone cortisol,30 with high levels in stressed or depressed people or extremely low levels in post-traumatic stress disorder (PTSD).31 In terms of serotonin we of course see low levels of it in depression32 and after bad experiences.33 Dopamine, central to the reward system and activated when we are positive, excited or eager, is another hormone that is profoundly affected by early experiences. Depressed mothers have low dopamine levels, and so do their babies as young as a month old. Thus not just our mental states but our brains and bodies adapt profoundly to our psychological context.
GENES, ENVIRONMENT, EPIGENETICS An important twist has been added to the adaptation story by the growing science of epigenetics which has shown how genes can either be expressed or silenced in response to particular kinds of experiences, via methylation (or demethylation) processes. Interestingly even brief stressful experiences in adults, such as a 90 min mock stressful job interview including difficult arithmetical questions, was shown to alter the action of a gene central to oxytocin production.34 Adverse early experiences have a more powerful effect on how genes are expressed.35 For example recent studies36 demonstrated that stress or trauma was correlated with higher methylation of a gene, exon 1F of NR3C1. More hopefully psychotherapy has been shown to positively affect gene expression, for example reducing the extent of methylation of the BDNF genes in adults who suffered childhood trauma.37 Experiences such as of trauma do not change the genes we inherit but they leave their mark, and indeed it seems that this Music G. Postgrad Med J 2016;92:128–133. doi:10.1136/postgradmedj-2015-133708
mark can transfer across generations, affecting how genes get expressed down the line.38 This has, for example, been seen in mice exposed to fearful experiences. When pups of these mice were exposed to the same stressor they showed fear, and the process whereby this occurred is DNA methylation.39 Holocaust survivors similarly seem to pass aspects of their stress response to their children via such processes.40 This again is adaptive, even if it smacks more of Lamarck41 than Darwin. If you live in a world where you expect trauma then you are more likely to survive if you are prepared, and in this case this survival and adaptation is enhanced by epigenetic mechanisms. What also is of interest is that some of us are more adaptable than others, or in other words some of us are less influenced by either good or bad experiences. This is called the ‘differential susceptibility to rearing hypothesis’.42 For example, if one has one of two versions of a dopamine receptor gene and has adverse early experiences then one’s outcomes (eg, mental health problems or increased risk taking) are likely to be worse.43 Similarly we can have one of two versions of the 5HT serotonin receptor gene, and those with the short version are more vulnerable to trauma and neglect,44 in the face of bad experiences being more prone to aggression, anxiety and depression. Such responsive and more easily influenced children are sometimes called ‘orchids’ as opposed to ‘dandelions’, as they grew particularly well only in special soil and do poorly in bad environments while the ‘dandelions’ grow anywhere. The orchids also benefit more from positive inputs such as therapeutic interventions.45 Thus some people are, for genetic reasons, more likely to be affected by both good and bad experiences.46 This raises interesting questions. The orchids may be more adaptive, which in some situations makes them more resilient and in others, less so.
LIFE HISTORY ADAPTATIONS We are all the time adapting to our environments, and this triggers neurobiological patterns that have a profound effect.47 Those born into highly stressed worlds tend to have a speeded up metabolism, faster heart rates, more activated stress response systems and develop, what some call, a fast as opposed to a slow life course strategy. We see this in a range of other mammals as well as humans, and it is a strategy that aids survival. We all have this in our evolutionary back-pocket, as otherwise any too trusting and complacent ancestors might well have met a violent end before they had time to reproduce. In some circumstances the best response is to be wary, vigilant and untrusting. Life history programming is so powerful that girls with insecure attachments tend to reach puberty earlier,48 as do those born into highly stressed families, or adopted from poor quality orphanages, or without fathers, and they are more likely to get involved in sexual activity younger, and reproduce earlier and more often.49 There is an evolutionary explanation for this which can only be speculative but which I think is plausible. In a dangerous world those who wait too long to reproduce might not survive long enough to do so, so starting early might aid passing on one’s genes.50 Perhaps this is why animals, including humans, tend to take more risks when their environments are unstable, becoming more involved in violence or promiscuity for example, and living a more highly stressed life. Research based on life history theory, propounded by many evolutionary psychologists,51 seems to be showing that if we are born into an environment where stress, anxiety, fear or trauma are likely, then we live a ‘faster life course’, and for example, breed earlier,48 take more risks and also die younger and have worse health along the way. Children with secure attachment 131
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PMJ 90th anniversary review styles, living in safe, relaxed environments, will non-consciously pick up very different messages, such as that it is sensible to wait longer to reproduce, it is safe to relax and trust the world, it is fine to have less children but to invest more in each one, and that one can rely on long-term stable relationships. When people are given cues that suggest a dangerous situation, those brought up in poorer socioeconomic circumstances tend to take more risks, while those brought up economically advantaged tend to take the slower, more risk-averse strategy.52 Unfortunately, while these neurobiological responses might be adaptive in that they aid survival, they have worrying longerterm sequelae. The classic study is a longitudinal one of over 17 000 people, called ACE, which measures averse childhood experiences,53 and people with the most adverse early experiences, such as of trauma, abuse or loss, end up suffering the worse health as they age, and indeed tend to die younger, often from diseases linked to metabolic syndrome.54 Such diseases, such as heart attacks, strokes and diabetes, are very linked with our stress responses. Thus a burgeoning body of research shows how exposure early on to stress has a profound physical effect, altering immune functioning, increasing the risk of all manner of diseases later on in life, including cancers. One study55 linked adverse experiences with issues ranging from increased smoking, alcohol and drug use, obesity and suicidality, all of which increased with more adverse experiences. Compared with persons with an ACE score of 0, those with an ACE score of 4 or more were twice as likely to be smokers, 12 times more likely to have attempted suicide, 7 times more likely to be alcoholic and 10 times more likely to have injected street drugs. A highly stressed life is also linked with a central telltale sign of physical ill-health and risk of early death, shorter telomeres.56 There appears to be a dose related response, so that the more the stress, the bigger effect on telomere length and the more likelihood of all kinds of diseases, from cancer to diabetes to heart disease.57 Indeed a recent study even found that stress in intrauterine life gave rise to shortened telomeres right up until adulthood.58 While at first glance such responses might seem maladaptive, what we see here is a tension between different options. A fast life course might be viewed as a kind of trade-off, sacrificing good health and longevity for immediate survival and a better chance of reproducing.59 This is an adaptive response, enhancing the passing on of genes successfully simply by increasing the chances of survival, but it is also a strategy that has lasting ill effects on psychological and physiological well-being.51
CONCLUSION The current story about adaptation has similar preoccupations to Crichton-Miller’s 1926 one in terms of working out how our nature adapts to our nurture.1 What has changed maybe, is our newer understanding of why certain seemingly maladaptive patterns might exist for good evolutionary and biological reasons. When Crichton-Miller suggests that the murderer is like the ‘infant of the human race’, and that many mentally ill are stuck in primitive functioning, his language may jar but perhaps in some ways his views are not so far away from contemporary ones. When under massive stress or feeling fearful we do, for example, rely on evolutionarily earlier aspects of our brains (eg, less prefrontal activation) and of our nervous systems (less reliance on ventral vagus system). Hypervigilance and alertness to potential danger would aid the chances of survival in frightening and uncertain environments. Similarly being emotionally cut-off helps survive in families where feelings are seen as bad. In tough, ruthless situations, 132
it does not pay to be kind and trusting, whereas being aggressive, selfish and ruthless might be more successful. Maybe what has changed since Crichton-Miller’s days is that we have begun to take the judgement out of our analysis and to take a more compassionate stance towards suffering and what some still see as maladaptation. While we live in a political climate in which criminality, the mentally unstable and even the poor are blamed for their plight, evolutionary theory is increasingly making sense of why such patterns might have adaptive origins. This should encourage us to argue for the conditions which would facilitate more health-inducing adaptations, such as those seen in securely attached, less stressed and more confident people.
Main messages ▸ Humans are highly adaptive, maybe more so than most species, and this extends to emotional adaptation. ▸ Behaviours that are adaptive in one context can become maladaptive in others. ▸ Adaptation occurs via the usual Darwinian selection processes. ▸ We also adapt due to having a range of potential pathways which can be turned on or off. ▸ Experiences affect our trajectory right down to a cellular level.
Current research questions ▸ Can early patterns be shifted, especially after trauma? ▸ What epigenetic effects might we see from positive experiences (such as therapy or adoption)? ▸ What responses to environmental impingements might start as adaptive and which might not? ▸ At what level ( psychological, bodily treatments, drugs, etc) might we make the most effective interventions?
Key references ▸ Hrdy SB. Mother Nature: Natural Selection and the Female of the Species. London: Chatto & Windus, 1999. ▸ Bowlby J. Attachment and loss. Volume 1 Attachment. London: Hogarth, 1969. ▸ McCrory E, De Brito SA, Viding E. Research review: the neurobiology and genetics of maltreatment and adversity. J Child Psychol Psychiatry 2010;51:1079–95. ▸ Music G. The Good Life: Wellbeing and the new science of altruism, selfishness and immorality. London: Routledge, 2014. ▸ Moule RK, Decker SH, Pyrooz DC. Social Capital, the Life-Course, and Gangs. Handb Life-Course Criminol 2013:143–58. Twitter Follow Graham Music at @grahammusic1 Competing interests None declared. Provenance and peer review Commissioned; externally peer reviewed. Music G. Postgrad Med J 2016;92:128–133. doi:10.1136/postgradmedj-2015-133708
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Adaptation: a contemporary view, revisiting Crichton-Miller's 1925 paper Graham Music Postgrad Med J 2016 92: 128-133 originally published online February 23, 2016
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