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CHAPTER 8
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Evolutionary
Contributions to the
Understanding of Mood
and Mood Disorders
Martin Brüne, M.D., Ph.D.
Daniel R. Wilson, M.D., Ph.D.
After the mind has suffered from an acute paroxysm of grief, and the cause still continues, we fall into a state of low spirits; or we may be utterly cast down and dejected. Prolonged bodily pain, if not amounting to an agony, generally leads to the same state of mind. If we expect to suffer, we are anxious; if we have no hope of relief, we despair.
Mood manages much of mammalian motivation. This is especially so in
the eusocial domain that operates above more ancient reptilian modes of agonic com­petition. Behavior of primates, particularly humans, is guided by brain systems that evolved over millions of years. Yet mood disorders, notably depression, are among the most common noncommunicable medical problems worldwide. How can this reality be reconciled with the view that the human body and mind were shaped by natural selection over eons of adaptation? Our answer is that neither the brain nor behavior was “designed” so much as accrued as a collection of all and sundry evolu-
Charles Darwin (1872)
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tionary adaptations to address diverse selective pressures. Thus, it is not surprising that regulation of mood is far from perfect. (We are unable to recap millions of years of evolutionary sculpting of mood and its disorders in a short chapter, so we posit some basic concepts. For more information, readers may consult other references, both supportive [as cited herein] and critical of our viewpoint [e.g., Confer et al. 2010; Plotkin 2004]).
In 2006 the World Health Organization predicted that by 2030, depression will con­stitute the second most burdensome disease (as measured in “years lived with disabil­ity”), surpassed only by HIV/AIDS but ranking before cardiovascular disease (Mathers and Loncar 2006; see also Chapter 3, “Epidemiology and Burden of Mood Disorders,” in this text). Notably, however, in contrast to cardiovascular disease, mood disorders usually affect people in the prime of life. What is low mood good for? Why is depres sion so widespread that in high-income countries, about one in four adults at some point will suffer a depressive episode? Why does depression commonly occur at an age at which the influence of selection is greatest—that is, near the peak of reproduc tive potential—unlike most other noncommunicable diseases, which increase with advanced age? Why is depression so readily elicited by the experience of adverse life events? Is there an intrinsic connection between rising incidence rates of depression worldwide and the decline of communicable (i.e., infectious) diseases, and if so, how can we make sense of it?
These are not the questions usually asked by clinicians or neuroscientists. Instead, low mood, or “spirit” as Darwin called it, is conventionally considered a psychologi cally painful condition that needs to be prevented because it is unpleasant and harm­ful. Accordingly, when studying more extreme forms of low mood, clinically labeled “depression,” neuroscientists seek to identify mechanisms that cause dysregulation of neurotransmission (e.g., low serotonin turnover in relation to genetic variation) and to determine functional and structural abnormalities in the brain (see Chapter 5, “Neuro­chemistry of Mood Disorders”; Chapter 9, “Anatomical Pathology”; “Brain Imaging”). Similarly, when neuroscientists ask why many psychiatric disorders emerge during adolescence and early adulthood, they typically attribute such risk to reorganization of the brain and/or hormonal changes, rather than considering the broader ramifications of what makes adolescence and young adulthood so special (Paus et al. 2008). Third, losses of important relationships and declines in social status are well known to precipitate depression, which, according to the conventional dia thesis-stress model (Monroe and Simons 1991), unfolds pathogenic potential via ge­netic vulnerability. But an important question is why these genes are so prevalent in the human gene pool. Finally, although the association of low mood and mood disorders with immunological activity has been well known for some time (Rook and Lowry
2009), inflammatory responses in depression are usually not considered in relation to epidemiological issues pertaining to infectious diseases. In sum, while clinical neuro­science explores important questions about the mechanistic causation of low mood and depression, it has paid insufficient attention to the evolved nature of the human mind.
This discrepancy in inquiry between neuroscience and evolutionary biology was long ago pointed out in a now famous article by Nobel Laureate Nicolaas Tinbergen (1963). Tinbergen made the distinction between “proximate” causation (mechanism and ontogeny) and “ultimate” or evolutionary causation (phylogeny and adaptive
and Chapter 11,
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value), each of which needs to be studied to fully understand any anatomical, physi­ological, or behavioral trait. Originally conceptualized to analyze animal anatomy and behavior, Tinbergen’s framework has been adopted to account for physical and psychological traits, including traits that at first sight appear dysfunctional (Brüne
2014). Thus, contrary to the view that an evolutionary approach to mood and mood disorders is reductionistic, such an approach is actually in full accord with a biopsy­chosocial model of health and disease (Engel 1977). Therefore, to give “ultimate” or evolutionary questions full credit, we emphasize in this chapter adaptationist perspec tives on excessively low and high mood (Nesse 2009; Wilson 2001). Specifically, we aim to review the most widely discussed evolutionary theories of mood and mood disorders, particularly the ones involving attachment and social competition; we fur ther explore the association of low mood with inflammation, discuss common genetic risk factors from an evolutionary vantage point, and present special aspects of mood disorders, including bereavement and suicidal behavior.
Evolutionary Principles for Understanding Mood and Mood Disorders
Ancestral Conditions and “Goals” of Evolution
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To appreciate what evolutionary biology can contribute to the understanding of mood and mood disorders—particularly the lingering question of why nature has left us vulnerable to depression, mania, and other psychiatric disorders—one needs to consider several issues. First, considering an evolutionary time frame is of particular importance. The human mind is endowed with cognitive, emotional, and behavioral capacities that emerged by natural and sexual selection at a time when our forebears lived as hunter-gatherers in close-knit communities, commonly referred to as an “en vironment of evolutionary adaptedness” (Bowlby 1969; Tooby and Cosmides 1990). This does not contradict recent evidence for ongoing selection in Homo sapiens (Stea rns et al. 2010), but our emotional life has probably changed very little since the Stone Age (Panksepp 2006). Ancestral environments were fraught with dangers, against which humans (and indeed our primate and mammalian ancestors) developed a broad array of defense mechanisms. These dangers ranged from microbial pathogens (even though—counterintuitively at first sight—the diversity of pathogens was prob­ably smaller than after domestication of animals) (Barnes 2005) to social threats, in­cluding competition for status and mates, as well as intertribal conflict (Gilbert et al.
2004). Therefore, evolved defenses include ones to fight infectious diseases, such as cough, fever, and inflammatory responses, as well as ones to minimize damage from social threats, including withdrawal, appeasement, and submission—or, conversely, to defend by way of social dominance. Whatever ancestral environments were specif ically like, however, they were in many respects fundamentally different from con­temporary conditions, and therefore our species experiences a range of phenotypic reactivity (Wilson 1998).
Second, although natural and sexual selection operate on the phenotype of any given trait, there is no “goal” in evolution apart from an anagenic tendency (an evolu­tionary trend from simpler to more complex forms) (Mayr 2001). Organisms do max-
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imize replication of genes, whereby the concept of kin selection refers to the replication of an individual’s genes shared with relatives of varying degree (Hamilton 1964). These technical statements have at least two important implications for the present chapter: 1) evolution does not specifically favor well-being or health, and 2) evolved traits are not optimal by design but rather are compromises of sometimes opposing selection pressures. Accordingly, low mood can be regarded as a defense against real or perceived environmental threats (i.e., a rescue strategy to preserve one’s reproduc tive potential), whereas high mood can be viewed as an effort to attain reproductive success via higher social rank. In the next section, we illustrate this principle of “de sign compromise” by describing the compromise with the furthest-reaching conse­quences for human mental life.
Life History Patterns and Human Attachment as a Design Compromise
Life history theory makes the point that organisms can invest in either somatic growth or reproduction, but not both simultaneously (Stearns 1992). Accordingly, there are two fundamentally different reproductive “strategies” (which here does not imply conscious choice): K-selected and r-selected strategies. Humans are among K-selected life forms, which grow larger-bodied, are slow to develop, reproduce repetitively, have few offspring per litter, care intensely for their young over long periods of time (which includes a long gestation period), and have relatively low death rates in in fancy and childhood. The onset of reproductive activity is delayed, and K-selected species usually enjoy long lives. Typically, social competition among adults is high, because—due to prolonged lifespans—success in intrasexual competition determines survival and reproductive success. K-selected species also usually live in conditions with little random environmental variation. A K-selected pattern is characteristic for primates, as well as for whales and elephants. In contrast, an r-selected strategy, which has characteristics that are opposite those described above, is the reproductive strategy for most insect and fish species, as well as (among mammals) small rodents (Stearns 1992).
In humans, the typical primate pattern is extended in all stages of development from infancy to adolescence and adulthood (Bogin 1999). It is important to note, how ever, that there is also within-species variation in life history strategies, commonly re­ferred to as the “pace of life.” In other words, some human life histories appear to be slightly more pushed to an r-selected-like pattern (“fast” life history), whereas others have a more extreme K-selected pattern (“slow” life history). Indeed, humans differ with regard to timing of biological maturation, age at onset of sexual activity and re­production, mating, number of offspring, and care provided for offspring (Ellis et al.
2011). These differences in “pace of life” critically depend on the nature of attachment patterns that develop during infancy and early childhood, whereby the special qual­ity of dyadic and triadic bonds between infant, mother, and father in terms of inten­sity and duration can be regarded as a design compromise par excellence.
Indeed, some 2.5 million years ago, environmental changes in East Africa were the starting point for a new way of locomotion in a clade of primates: bipedalism. Al­though the selection pressures that caused upright walking are still debated (Preu­schoft 2004), as selection favored the evolution of larger brains in bipedal hominins,
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probably due to the demands of increasingly complex social structures (Dunbar and Shultz 2007), giving birth to immature offspring emerged as a design compromise to accommodate a narrow pelvis, a situation termed the “obstetric dilemma” (Wells et al. 2012). However, not only brain size (and hence head circumference) mattered, but also the nutritional demands of a large brain that could not be supplied by the mater nal placenta for longer than 9 months (Campbell 2010). These circumstances, in turn, created new selective pressures on parenting and mating. If humans were born as ma turely as our closest extant relatives, the great apes, pregnancy would last 22 months. Human immaturity at birth necessitated particular adaptations in mother-infant bonding; because mothers were less capable of foraging when caring for immature babies, there was a need for increasing paternal and close kin investment, allowing “cooperative breeding” (Hrdy 2000).
The mechanism through which dyadic and triadic relationships between infant, mother, and father develop is known as “attachment.” Bowlby (1969) discovered that human newborns, like other primates and perhaps all mammals, are “preprogrammed” to seek proximity to caregivers as a way to secure their own survival. Evolutionarily speaking, it is in the genetic interest of mothers and fathers to be highly responsive to their babies’ needs (Hamilton 1964). However, attachment is not only about food and security. Rather, it is also about the caregiver’s emotional availability, which is decisive for the development of a child’s “internal working model” about the world. A child who can rely on trustworthy and responsive care is more likely to perceive the world as a safe place. Conversely, if caregivers are less willing or able to emotionally respond to infants’ needs, insecure attachment may cause infants to perceive the world as dan­gerous (Bowlby 1969). Impending abandonment is a life-threatening condition in the environment of evolutionary adaptedness, in which young infants typically display separation distress and anxiety. If separation continues, infants go through phases of protest, despair, and detachment, typically associated with low mood. Prolonged sep­aration, such as for hospitalized infants, may cause “anaclitic” depression (Spitz 1945).
Although Bowlby (1969) believed that only secure attachment could be adaptive, more recent work suggests that fluctuations in ancestral environmental conditions in terms of resource availability have selected for a set of flexible adaptive behavioral re­sponses to accomplish important biosocial goals (Simpson 1999). For example, when confronting harsh environmental conditions, which may include food scarcity or lack of emotional availability of caregivers, an individual is more likely to develop an inter­nal working model that the world is unsafe and future resources are uncertain, so that immediate resource extraction might be the best strategy. Such strategies may include exploitation of others with an opportunistic interpersonal style, more risk-prone be haviors, early mating efforts with limited investment in offspring, and even the accel­eration of biological maturation, thus driving the “pace of life” slightly into a “faster” direction (Belsky 1999). Insecure attachment therefore reflects, to some extent, a prox­imate adaptive strategy evolved to ensure survival and to maximize reproductive suc­cess under unpredictable environmental conditions. However, as the likelihood of not reaching significant goals also increases, it is plausible to assume that a “faster” pace of life is associated with an increased risk for psychopathology, including depression and mania (Brüne 2016a; Del Giudice 2014; Hurst and Kavanagh 2017). Such individ­ual differences are observable to the present day, in that poverty and social inequality leave their marks on individual pace of life (Hochberg and Belsky 2013).
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Biosocial Goals
In addition to care-eliciting and caregiving (the major concerns of attachment and bonding), humans pursue other biosocial goals that, from an evolutionary point of view, are critical for the sake of survival and reproductive success (Gilbert and Allan
1998). These goals embrace mate selection and mating, formation of alliances, and rank in the social hierarchy. This formulation is so general that it applies to virtually all social species; however, the increasing complexity of human sociality has brought about a sophisticated set of emotions and cognitive abilities that evolved to maintain cooperation and reciprocal relationships in tribal societies (Trivers 1971). In fact, mu­tual dependence (including food sharing), caring for sick or otherwise incapacitated individuals, sharing of knowledge, and other forms of altruistic behaviors were so imperative in ancestral societies that tendencies of “free riding” or cheating had to be controlled. Such a scenario has most likely contributed to the evolution of rewarding emotions such as friendship, sympathy, trust, and gratitude; in addition, negative emotions, including shame and guilt, emerged in response to the need for reconcilia­tion when cooperation was violated (Trivers 1971). Given the complexity of human social life, it is almost inconceivable that biosocial goals and rules of cooperation and reciprocity are never thwarted or violated. Instead, the experience of social goals ob­structed by one’s own or others’ failure is so common that low mood is an inevitable part of human nature. Moreover, as evolutionary analysis of low mood and mood dis orders suggests, guilt and shame are intricately linked with phenotypic expressions of depression (Panksepp 2006).
In summary, there are several evolutionary explanations as to why the human mind is left vulnerable to developing low mood and mood disorders (Gilbert and Allan 1998; Wilson 1998): 1) environmental mismatch and phenotypic plasticity (i.e., ances­tral environments, including the pathogenic landscape, are different from contempo­rary ones); 2) selection favors reproductive success but not well-being; 3) psychological features, like anatomical traits, are design compromises; 4) moods (including some ex treme variants) are defense mechanisms and thus part of human nature; and 5) the thwarting of biosocial goals is inevitable. All of this leads to the question of what low and high mood could be good for.
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Evolutionary Theories of Mood and Mood Disorders
The concept of “mood” is intricately linked to the concepts of “emotions” and “feel­ings,” and the terms are often used interchangeably. However, the difference between the concepts of “mood” and “emotions” is more akin to that between “climate” and “weather.” That is, in contrast to acute emotions, mood is a more pervasive state, partly detached from immediate environmental stimuli (Nettle and Bateson 2012). As mood emerges from recurrent experiences of emotional responses to specific triggers associated with reward or punishment, it can adjust the threshold for detection of fu­ture incentives or threats. Possessing a “mood system” is thus adaptive, because it can direct attention and vigilance toward the approach of rewarding events or avoidance of punishing events. The absence of reward, for example, causes low (or depressed) mood and raises the threshold for reward-seeking behavior, whereas repeated punish-
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ment (or continuous exposure to danger) initiates avoidance behavior through anx­ious mood states (Nettle and Bateson 2012), and avidity for reward can drive hypo­mania and mania (Wilson 1998). Emotions are commonly elicited by exteroceptive input (i.e., vision, audition, odor, taste, or tactile sensation) that can elicit feelings— that is, the subjective experiences accompanying emotional states. Conversely, some feelings (e.g., hunger and thirst) need not necessarily be caused by emotions (Dama sio and Carvalho 2013).
Mood is a phylogenetically old adaptation that helps guide organismic behavior based on the estimated likelihood that a particular situation will recur. More specifi cally, low mood can be regarded as an evolved defense mechanism that protects the organism against ongoing exposure to fitness-reducing environmental contingencies. Although low mood is subjectively unpleasant and undesirable, it is an important signal to the organism to pause, save energy, and reevaluate the situation in order to recuperate homeostasis. On the other end of the scale, high mood can propel organ isms toward resources and social rank.
Excessive low mood is commonly associated with a diagnosis of clinical depression, and excessive high mood with mania. The excess can pertain to the intensity, duration, or both. Evolutionary perspectives on mood disorders would argue that there is no clear boundary between “normal” mood and pathological extremes (Brüne 2016b; Nettle and Bateson 2012). However, even though it is disputed by some evolutionary scientists, our standpoint is that at least severe states of clinical depression and mania are maladaptive in the Darwinian sense. Moreover, these likely are more common in the modern ontogenic environment than they were in the environment of evolutionary adaptedness. The analogy to cough and fever may illustrate this stance: these defenses against attacks of pathogenic agents are clearly adaptive if they help expel or kill vi­ruses or microbes. Excessive cough or septic fever, however, can cause severe damage or even death. Likewise, (severe) depression or mania is detrimental to biological fit ness and may cause significant disability (Wilson 1998). Given the vast number of life events that can cause mood variation, depression, or mania, we look at specific evo lutionary explanations for mood and mood disorders.
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Attachment Theory Perspective
Darwin’s statement heading this chapter alluded to a common cause of depression, namely the loss of an important relationship. Darwin’s deep insights foreshadowed the typical stages of low mood following separation from an attachment figure (Bowlby 1969). In fact, young mammals, when abandoned, are exposed to several risks, such as predation, starvation, or perishing from cold. Accordingly, a first re sponse to abandonment is protest, by which the young signal distress to reinforce re­union with the attachment figure. This response is typically associated with communi­cative signals of low mood—vocally by crying, and facially by the expression of anger. In addition, locomotor activity in search of the attachment figure can occur. Prolonged protesting, however, is perilous itself, because it may attract predators or lead to ex­haustion. Therefore, after some time, protest ceases, giving way to a phase of despair. Despair is adaptive in situations in which rapid reunion is precluded. The young thus stops signaling. Instead, it immobilizes, turns mute, and changes facial expression to sadness/despair (for an overview, see Gilbert 2006). Darwin already noted “the
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