Early adversity is a major risk factor for the emergence of psychopathology across development. Identifying mechanisms that support resilience, or favorable mental health outcomes despite exposure to adversity, is critical for informing clinical intervention and guiding policy to promote youth mental health. Here we propose that caregivers play a central role in fostering resilience among children exposed to adversity via caregiving influences on children’s corticolimbic circuitry and emotional functioning. We first delineate the numerous ways that caregivers support youth emotional learning and regulation and describe how early attachment lays the foundation for optimal caregiver support of youth emotional functioning in a developmental stage-specific manner. Second, we outline neural mechanisms by which caregivers foster resilience—namely, by modulating offspring corticolimbic circuitry to support emotion regulation and buffer stress reactivity. Next, we highlight the importance of developmental timing and sensitive periods in understanding caregiving-related mechanisms of resilience. Finally, we discuss clinical implications of this line of research and how findings can be translated to guide policy that promotes the well-being of youth and families.
Adverse ecological and social conditions during early life are known to influence development, with rippling effects that may explain variation in adult health and fitness. The adaptive function of such developmental plasticity, however, remains relatively untested in long‐lived animals, resulting in much debate over which evolutionary models are most applicable. Furthermore, despite the promise of clinical interventions that might alleviate the health consequences of early‐life adversity, research on the proximate mechanisms governing phenotypic responses to adversity have been largely limited to studies on glucocorticoids. Here, we synthesize the current state of research on developmental plasticity, discussing both ultimate and proximate mechanisms. First, we evaluate the utility of adaptive models proposed to explain developmental responses to early‐life adversity, particularly for long‐lived mammals such as humans. In doing so, we highlight how parent‐offspring conflict complicates our understanding of whether mothers or offspring benefit from these responses. Second, we discuss the role of glucocorticoids and a second physiological system—the gut microbiome—that has emerged as an additional, clinically relevant mechanism by which early‐life adversity can influence development. Finally, we suggest ways in which nonhuman primates can serve as models to study the effects of early‐life adversity, both from evolutionary and clinical perspectives.
more » « less- PAR ID:
- 10460533
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Evolutionary Anthropology: Issues, News, and Reviews
- Volume:
- 28
- Issue:
- 5
- ISSN:
- 1060-1538
- Page Range / eLocation ID:
- p. 249-266
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
null (Ed.)Residence at high altitude is consistently associated with low birthweight among placental mammals. This reduction in birthweight influences long-term health trajectories for both the offspring and mother. However, the physiological processes that contribute to fetal growth restriction at altitude are still poorly understood, and thus our ability to safely intervene remains limited. One approach to identify the factors that mitigate altitude-dependent fetal growth restriction is to study populations that are protected from fetal growth restriction through evolutionary adaptations (e.g., high altitude-adapted populations). Here, we examine human gestational physiology at high altitude from a novel evolutionary perspective that focuses on patterns of physiological plasticity, allowing us to identify 1) the contribution of specific physiological systems to fetal growth restriction and 2) the mechanisms that confer protection in highland-adapted populations. Using this perspective, our review highlights two general findings: first, that the beneficial value of plasticity in maternal physiology is often dependent on factors more proximate to the fetus; and second, that our ability to understand the contributions of these proximate factors is currently limited by thin data from altitude-adapted populations. Expanding the comparative scope of studies on gestational physiology at high altitude and integrating studies of both maternal and fetal physiology are needed to clarify the mechanisms by which physiological responses to altitude contribute to fetal growth outcomes. The relevance of these questions to clinical, agricultural, and basic research combined with the breadth of the unknown highlight gestational physiology at high altitude as an exciting niche for continued work.more » « less
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Abstract Phenotypic variation within populations is influenced by the environment via plasticity and natural selection. How phenotypes respond to the environment can vary among traits, populations and life stages in ways that can influence fitness.
Plastic responses during early development are particularly important because they can affect components of fitness throughout an individual's life. Consequently, how natural selection shapes developmental plasticity could be influenced by fitness consequences across different life stages. Moreover, spatial variation in selection pressures could generate differences in plastic responses among populations.
To gain insight into sources of variation in phenotypes and survival, we used a laboratory egg incubation experiment using brown anole lizards
Anolis sagrei from mainland (ancestral) and island (descendent) populations, combined with a mark–release–recapture experiment in the field. Our study was designed to (a) quantify the effects developmental temperature on embryo development and offspring morphology, (b) assess how developmental temperature influences offspring survival across different life stages and (c) quantify how thermal reaction norms vary among ancestral and descendant populations.Developmental temperature influenced offspring morphology, but thermal reaction norms of embryos showed little variation among populations. Developmental temperature influenced offspring survival, but the patterns differed between embryo and hatchling stages; the optimal temperature for embryos was about 5℃ lower than that for hatchlings. High temperatures were thermally stressful to embryos, but they reduced incubation duration and led to early hatching. In turn, earlier hatching increased the probability of survival to adulthood. Moreover, the effect of developmental temperature on hatchling survival was most pronounced for offspring that hatched late in the season.
The difference in optimal developmental temperatures between life stages may be driven by physiological tolerance for embryos and by ecological factors for hatchlings. Moreover, the fitness consequences of the developmental environment depend on the phenology of hatching. Overall, these results highlight how the developmental environment can differentially affect fitness across life stages and show that temporal thermal heterogeneity can influence survival of embryos, but the consequences on post‐hatching stages may vary at different times of the season.
A free
Plain Language Summary can be found within the Supporting Information of this article. -
ABSTRACT As a response to environmental cues, maternal glucocorticoids (GCs) may trigger adaptive developmental plasticity in the physiology and behavior of offspring. In North American red squirrels (Tamiasciurus hudsonicus), mothers exhibit increased GCs when conspecific density is elevated, and selection favors more aggressive and perhaps more active mothers under these conditions. We tested the hypothesis that elevated maternal GCs cause shifts in offspring behavior that may prepare them for high-density conditions. We experimentally elevated maternal GCs during gestation or early lactation. We measured two behavioral traits (activity and aggression) in weaned offspring using standardized behavioral assays. Because maternal GCs may influence offspring hypothalamic–pituitary–adrenal (HPA) axis dynamics, which may in turn affect behavior, we also measured the impact of our treatments on offspring HPA axis dynamics (adrenal reactivity and negative feedback), and the association between offspring HPA axis dynamics and behavior. Increased maternal GCs during lactation, but not gestation, slightly elevated activity levels in offspring. Offspring aggression and adrenal reactivity did not differ between treatment groups. Male, but not female, offspring from mothers treated with GCs during pregnancy exhibited stronger negative feedback compared with those from control mothers, but there were no differences in negative feedback between lactation treatment groups. Offspring with higher adrenal reactivity from mothers treated during pregnancy (both controls and GC-treated) exhibited lower aggression and activity. These results suggest that maternal GCs during gestation or early lactation alone may not be a sufficient cue to produce substantial changes in behavioral and physiological stress responses in offspring in natural populations.more » « less
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Rationale Early life social rearing has profound consequences on offspring behavior and resilience. Yet, most studies examining early life development in rodents use species whose young are born immobile and do not produce complex social behavior until later in development. Furthermore, models of rearing under increased social complexity, rather than deprivation, are needed to provide alternative insight into the development of social neural circuitry. Objectives To understand precocial offspring social development, we manipulated early life social complexity in the communal spiny mouse Acomys cahirinus and assessed long-term consequences on offspring social behavior, exploration, and neural responses to novel social stimuli. Methods Spiny mouse pups were raised in the presence or absence of a non-kin breeding group. Upon adulthood, subjects underwent social interaction tests, an open field test, and a novel object test. Subjects were then exposed to a novel conspecific and novel group and neural responses were quantified via immunohistochemical staining in brain regions associated with social behavior. Results Early life social experience did not influence behavior in the test battery, but it did influence social processing. In animals exposed to non-kin during development, adult lateral septal neural responses toward a novel conspecific were weaker and hypothalamic neural responses toward a mixed-sex group were stronger. Conclusions Communal species may exhibit robust behavioral resilience to the early life social environment. But the early life environment can affect how novel social information is processed in the brain during adulthood, with long-term consequences that are likely to shape their behavioral trajectory.more » « less
