Why and how does early adversity influence development? Toward an integrated model of dimensions of environmental experience. Bruce J. Ellis, Margaret A. Sheridan, Jay Belsky and Katie A. McLaughlin. Development and Psychopathology, Mar 14 2022. https://doi.org/10.1017/S0954579421001838
Abstract: Two extant frameworks – the harshness-unpredictability model and the threat-deprivation model – attempt to explain which dimensions of adversity have distinct influences on development. These models address, respectively, why, based on a history of natural selection, development operates the way it does across a range of environmental contexts, and how the neural mechanisms that underlie plasticity and learning in response to environmental experiences influence brain development. Building on these frameworks, we advance an integrated model of dimensions of environmental experience, focusing on threat-based forms of harshness, deprivation-based forms of harshness, and environmental unpredictability. This integrated model makes clear that the why and the how of development are inextricable and, together, essential to understanding which dimensions of the environment matter. Core integrative concepts include the directedness of learning, multiple levels of developmental adaptation to the environment, and tradeoffs between adaptive and maladaptive developmental responses to adversity. The integrated model proposes that proximal and distal cues to threat-based and deprivation-based forms of harshness, as well as unpredictability in those cues, calibrate development to both immediate rearing environments and broader ecological contexts, current and future. We highlight actionable directions for research needed to investigate the integrated model and advance understanding of dimensions of environmental experience.
Integrative discussion of harshness and deprivation
In addition to harm imposed by other agents, insufficient environmental inputs (material, energetic, or social) was another important source of harshness over human evolutionary history (Frankenhuis & Amir, Reference Frankenhuis and Amir2021). In this section, we focus on the adaptive problem of insufficient environmental inputs – a distinct set of selection pressures posed by the environment – and how developmental systems evolved to detect and respond to cues indicating the presence of this adaptive problem (Figure 1).
In early childhood, experiences of deprivation are often mediated through caregiver behavior, which is responsive to larger ecological conditions such as social/alloparental support, socioeconomic adversity, pathogen stress, and community-level violence (Belsky, Reference Belsky1984; Belsky et al., Reference Belsky, Steinberg and Draper1991; Eltanamly et al., Reference Eltanamly, Leijten, Jak and Overbeek2021; Quinlan, Reference Quinlan2007). The quantity and quality of interactions with caregivers contributes to early childhood experiences of deprivation. In traditional human societies, and by inference over human evolutionary history, some caregiver-mediated forms of deprivation (e.g., early weaning, low provisioning of food, low sleeping proximity to infants, reduced carrying of children, and caregiver neglect) increase childhood morbidity–mortality risk from causes such as malnutrition, disease, physical exposure, predation, and conspecific violence (Frankenhuis & Amir, Reference Frankenhuis and Amir2021; Quinlan, Reference Quinlan2007; Volk & Atkinson, Reference Volk and Atkinson2008, Reference Volk and Atkinson2013). For example, in traditional human societies, maternal mortality has catastrophic and universally negative effects on the survival of young children prior to weaning age (Sear & Mace, Reference Sear and Mace2008). From this perspective, significant experiences of deprivation (especially deprivation experiences that were reliably associated with morbidity–mortality over evolutionary history) are nested within harshness (Figure 1). Our developmental systems should have evolved to detect and respond to these forms of deprivation.Footnote4
Like cues to threat-based forms of harshness, cues to deprivation-based forms of harshness vary from more proximal to the child (e.g., caregiver neglect, limited social or cognitive input, food scarcity, homelessness and other forms of material deprivation) to more distal to the child (e.g., famine, drought, resource shortages, unemployment, and poverty). Proximal cues correspond to the concept of deprivation in the threat-deprivation model: infrequent or low-quality environmental inputs experienced by the child. Distal cues reflect ecological factors linked to deprivation. As shown in Figure 1, distal cues may signal morbidity–mortality risk from insufficient environmental inputs either directly or indirectly (through proximal cues).
In this paper, we have stipulated that threat-based forms of harshness (as well as unpredictability) both constrain development and regulate it toward strategies that are adaptive under stressful conditions. These adaptive arguments postulate that developmental adaptations to adversity evolved in response to environmental variation and function to match the developing phenotype to relevant conditions. Such arguments may be less applicable to deprivation, however, especially in its more severe forms. In many cases, developmental responses to deprivation can be more parsimoniously explained as attempts to spare or preserve function. Such responses may enable individuals to make the best of bad circumstances in the context of substantial developmental constraints (i.e., low survival, poor growth, reduced reproduction; see Bogin et al., Reference Bogin, Silva and Rios2007) imposed by deprivation-mediated tradeoffs. Making the best of bad circumstances means that individuals adjust their phenotypes to the deprived conditions under which they are developing – allowing them to achieve better survival and reproductive outcomes than if they did not adjust their phenotypes – but still fare worse than peers who did not experience deprivation. In this section, we consider such tradeoffs from the perspective of life history theory. We propose that (a) deprivation-mediated tradeoffs fundamentally involve sacrificing growth to reduce maintenance costs, and that such tradeoffs occur in response to both energetic deprivation (central to the harshness-unpredictability framework) and social/cognitive deprivation (central to the threat-deprivation framework); and (b) individuals mount responses to deprivation that enable them to make the best of bad circumstances.
Energetic deprivation
A major form of deprivation is nutritional, or energetic deprivation. Within a life history framework, a central assumption is that natural selection has favored physiological mechanisms that track variation in energetic conditions (i.e., resource availability, energy balance, and related physical condition) and adjust growth to match that variation (Ellis, Reference Ellis2004; Ellison, Reference Ellison2003). Consequently, a central resource-allocation tradeoff, beginning in the prenatal period, is between maintenance and growth (for an extensive review, see Bogin et al., Reference Bogin, Silva and Rios2007). A baseline level of energy expenditure is needed to maintain basic functioning and repair or preserve the soma (e.g., brain metabolism, digestion, immune function, cellular/DNA repair, pathogen and predator defenses). Above these baseline investments in maintenance, resources can be allocated to growth and eventually reproduction. Growth builds capacities that enhance overall reproductive potential; it encompasses developmental processes and activities that increase physical size as well as social and cognitive competencies (e.g., development of abstract information-processing capacities, acquisition of skills and knowledge).
Consistently enriched or supportive conditions in early and middle childhood may signal to the individual that investments in growth are sustainable. Conversely, conditions of chronic resource scarcity may shift individuals toward development of an energy-sparing phenotype that economizes somatic maintenance costs by limiting growth. Energetic deprivation was a common feature of ancestral human environments. In subsistence-level populations, low energy availability co-occurs with both periods of negative energy balance (when caloric expenditures exceed caloric intake) and high pathogen burden/immunological challenges (e.g., McDade, Reference McDade2003; Urlacher et al., Reference Urlacher, Ellison, Sugiyama, Pontzer, Eick, Liebert, Cepon-Robins, Gildner and Snodgrass2018). Energetic deprivation, as instantiated in this co-occurring set of conditions, is associated with slower growth, later sexual maturation, and smaller body size (e.g., Bogin et al., Reference Bogin, Silva and Rios2007; Ellis, Reference Ellis2004; Ellison, Reference Ellison2003); relatively low progesterone concentrations and reduced fecundity in women (Ellison, Reference Ellison2003; Jasienska et al., Reference Jasienska, Bribiescas, Furberg, Helle and Núñez-de la Mora2017); and relatively low testosterone concentrations and reduced skeletal muscle tissue in men (Bribiescas, Reference Bribiescas2001, Reference Bribiescas2010). These adjustments of life history-related traits to chronic ecological conditions are generally considered an example of adaptive phenotypic plasticity (Ellison, Reference Ellison2003; Ellis, Reference Ellis2004). In this case, energetic deprivation regulates development toward a slower life history strategy that is maintenance-cost-effective: growth is constrained, and reproductive capacity is achieved later in development.
Although energetic deprivation constrains growth and reproductive maturation, individuals should still mount responses to energetic deprivation that enable them to make the best of bad circumstances. Energetic deprivation, and the closely related conditions of pathogen stress (e.g., McDade, Reference McDade2003; Urlacher et al., Reference Urlacher, Ellison, Sugiyama, Pontzer, Eick, Liebert, Cepon-Robins, Gildner and Snodgrass2018) and warfare related to food shortages/food instability (Ember & Ember, Reference Ember and Ember1992), were major co-occurring causes of extrinsic morbidity–mortality over evolutionary history. These co-occurring environmental factors may have opposing effects on the development of life history strategies. Like developmental exposures to threat, cues to high pathogen stress (e.g., high local fatality rates from infectious disease) predict faster life history-related traits (Lu et al., Reference Lu, Wang, Liu and Chang2021; Quinlan, Reference Quinlan2007).Footnote5 This means that shifts toward slower life history strategies induced by energetic deprivation often occur in the context of countervailing shifts toward faster life history strategies in response to cues to extrinsic morbidity–mortality from other sources. For example, in a comparison of 22 small-scale human societies (hunter–gatherers and subsistence-based horticulturalists), poor energetic conditions were associated with later ages of menarche and first birth, whereas higher childhood mortality rates were associated with earlier ages of menarche and first birth (Walker et al., Reference Walker, Gurven, Hill, Migliano, Chagnon, De Souza, Djurovic, Hames, Hurtado, Kaplan, Kramer, Oliver, Valeggia and Yamauchi2006). Likewise, in cohort studies in Estonia, the Philippines, and Brazil, complex adversity exposures involving energetic deprivation together with other forms of harshness or unpredictability (e.g., poverty, parental instability, sibling death) predicted both later pubertal development and earlier ages at first reproduction (Gettler et al., Reference Gettler, McDade, Bragg, Feranil and Kuzawa2015; Hõrak et al., Reference Hõrak, Valge, Fischer, Mägi and Kaart2019; Valge et al., Reference Valge, Meitern and Hõrak2021; Wells et al., Reference Wells, Cole, Cortina-Borja, Sear, Leon, Marphatia, Murray, Wehrmeister, Oliveira, Gonçalves, Oliveira and Menezes2019). In the Brazilian cohort, other shifts toward faster life history-related traits were also observed, including greater risky behavior indicative of future discounting (i.e., smoking, criminal behavior) (Wells et al., Reference Wells, Cole, Cortina-Borja, Sear, Leon, Marphatia, Murray, Wehrmeister, Oliveira, Gonçalves, Oliveira and Menezes2019). In total, the literature on energetic deprivation in the context of harshness/unpredictability provides a textbook case of the complex – and sometimes countervailing nature – of developmental responses to adversity. Despite the negative effects of energetic deprivation on growth, broader phenotypic responses may still make the best of bad circumstances. Within ecological constraints, that potentially involves diverting resources toward earlier reproduction, as well as other shifts toward faster life history-related traits, particularly in relation to other cues to extrinsic morbidity–mortality or unpredictability.
Social/cognitive deprivation
The complex effects of energetic deprivation on reproductive development and behavior provide a model for considering the effects of social/cognitive deprivation on neurodevelopment and learning. Our developmental systems may have evolved to treat experiences of deprivation as privileged sources of information, using them as a basis for implementing developmental tradeoffs favoring maintenance over growth. Such tradeoffs fundamentally concern neurodevelopment, given the unusually high energetic costs of the human brain. Indeed, glucose consumed by the brain accounts for roughly 66% of the body’s resting metabolic rate and 43% of total energy expenditure in middle childhood (Kuzawa et al., Reference Kuzawa, Chugani, Grossman, Lipovich, Muzik, Hof, Wildman, Sherwood, Leonard and Lange2014). This high energetic cost reflects the size and complexity of the human brain, with its trillions of functional connections. Achieving high levels of neural complexity is costly – in terms of time, energy, and risk – and, critically, depends on adequate parental investment and social support (Snell-Rood & Snell-Rood, Reference Snell-Rood and Snell-Rood2020).
When such investment and support is lacking from the environment, one result may be reduced investment in neural development. Indeed, social and cognitive deprivation related to institutionalization, neglect, and other environments characterized by low levels of cognitive stimulation, such as lower socioeconomic status, have been consistently linked to reductions in brain volume, cortical surface area, and cortical thickness in children and adolescents. Reduced cortical volume, surface area, and thickness in children who have experienced deprivation are global, widespread, and occur not only in regions of association cortex but also in sensory cortex (Hanson, Hair et al., Reference Hanson, Hair, Shen, Shi, Gilmore, Wolfe and Pollak2013; Herzberg et al., Reference Herzberg, Hodel, Cowell, Hunt, Gunnar and Thomas2018; Hodel et al., Reference Hodel, Hunt, Cowell, Van Den Heuvel, Gunnar and Thomas2015; Mackey et al., Reference Mackey, Finn, Leonard, Jacoby-Senghor, West, Gabrieli and Gabrieli2015; McLaughlin, Sheridan, Winter et al., Reference McLaughlin, Sheridan, Winter, Fox, Zeanah and Nelson2014; Noble et al., Reference Noble, Houston, Brito, Bartsch, Kan, Kuperman, Akshoomoff, Amaral, Bloss, Libiger, Schork, Murray, Casey, Chang, Ernst, Frazier, Gruen, Kennedy, Van Zijl, Mostofsky and Sowell2015; Sheridan et al., Reference Sheridan, Fox, Zeanah, McLaughlin and Nelson2012). The precise cellular mechanisms contributing to thinner cortex, and whether these patterns reflect an acceleration or delay in neurodevelopment, remains unknown. Social/cognitive forms of deprivation in early life are also associated with reductions in the integrity of structural connections between brain areas across a wide range of white matter tracts (Eluvathingal et al., Reference Eluvathingal, Chugani, Behen, Juhasz, Muzik and Maqbool2006; Govindan et al., Reference Govindan, Behen, Helder, Makki and Chugani2010; Hanson, Adluru et al., Reference Hanson, Adluru, Chung, Alexander, Davidson and Pollak2013; Rosen et al., Reference Rosen, Sheridan, Sambrook, Meltzoff and McLaughlin2018). In total, substantial evidence suggests that deprivation in childhood is associated with a pattern of neurodevelopment that results in a smaller brain, as reflected by global reductions in cortical gray matter volume, surface, and thickness, as well as brain that is less connected, as revealed by a global decrease in the structural integrity of white matter tracts.
Deprivation-mediated reductions in neural growth and structural connectivity have been hypothesized to result in lower brain metabolic rates (Snell-Rood & Snell-Rood, Reference Snell-Rood and Snell-Rood2020). Thus, social/cognitive deprivation, like energetic deprivation, may shift individuals toward development of a maintenance-cost effective phenotype by constraining neural development. Stated differently, the effects of energetic and social/cognitive deprivation can be understood in terms of the same underlying tradeoff favoring maintenance over growth.
Research conducted within the threat-deprivation framework, and in developmental cognitive neuroscience more generally, has taken a deficit-based approach to deprivation. This is understandable, given the well-documented associations between social/cognitive deprivation and constraints on neurodevelopment and learning (see above, The Threat-Deprivation Framework). Nonetheless, an evolutionary-developmental perspective implies that children mount responses to deprivation that make the best of bad circumstances (see Ellis et al., Reference Ellis, Abrams, Masten, Sternberg, Tottenham and Frankenhuis2020). Such responses may involve the development of stress-adapted skills, or “hidden talents,” that enable adaptation within high-adversity contexts (Ellis et al., Reference Ellis, Bianchi, Griskevicius and Frankenhuis2017; Frankenhuis & de Weerth, Reference Frankenhuis and de Weerth2013), including rearing environments characterized by deprivation. Homeless youth, for example, generally experience considerable social, cognitive, and material deprivation. Although homeless youth tend to perform worse than comparison youth on executive function tasks, they have been found to perform as well or better on tests of creativity (Dahlman et al., Reference Dahlman, Bäckström, Bohlin and Frans2013; Fry, Reference Fry2018). Heightened creativity in the context of homelessness is presumably a stress-adapted skill for solving problems relevant to surviving in a deprived and unpredictable environment. Likewise, in explore-exploit decision-making tasks, previously institutionalized children use more exploitative strategies than peers raised in families (Humphreys et al., Reference Humphreys, Lee, Telzer, Gabard-Durnam, Goff, Flannery and Tottenham2015; Kopetz et al., Reference Kopetz, Woerner, MacPherson, Lejuez, Nelson, Zeanah and Fox2019; Loman et al., Reference Loman, Johnson, Quevedo, Lafavor and Gunnar2014). This exploitive strategy was detrimental under forgiving experimental conditions, but beneficial when conditions become harsh (i.e., when parameters of the task changed to hasten punishment) (Humphreys et al., Reference Humphreys, Lee, Telzer, Gabard-Durnam, Goff, Flannery and Tottenham2015). More generally, children exposed to deprived (as well as threatening) early environmental conditions – poverty, maternal disengagement, high neighborhood crime – may develop enhanced problem-solving skills for extracting fleeting or unpredictable rewards from the environment (Li et al., Reference Li, Sturge-Apple and Davies2021; Sturge-Apple et al., Reference Sturge-Apple, Davies, Cicchetti, Hentges and Coe2017; Suor et al., Reference Suor, Sturge-Apple, Davies and Cicchetti2017). Research documenting such hidden talents, however, does not condone exposing children to experiences that are obviously impairing in modern life. Instead, observations of how neural and cognitive function adapt to harsh early circumstances may support a strengths-based approach to intervention that leverages stress-adapted skills (Ellis et al., Reference Ellis, Bianchi, Griskevicius and Frankenhuis2017, Reference Ellis, Abrams, Masten, Sternberg, Tottenham and Frankenhuis2020).
Directions for future research
Little attempt has been made to study the potentially opposing effects of energetic deprivation and other forms of harshness on life history-related traits, or to link the patterns of cognitive and neurodevelopment associated with social/cognitive deprivation with life history traits. These represent obvious avenues for future research to investigate the ideas advanced here. Research is also needed to test the “maintenance-cost effective phenotype” hypothesis, especially in relation to neural development. See Table 2 for more specific directions for future research.
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