Developmental responses to early‐life adversity: Evolutionary and mechanistic perspectives

Abstract

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.

Effects of early life adversity on maternal effort and glucocorticoids in wild olive baboons

“…Maternal GCs are a key signal orchestrating offspring phenotype (Allen-Blevins et al, 2015;Lu et al, 2019). Early life adversity has programming effects on neuroendocrine functioning and epigenetic changes to genes involved with HPA-axis regulation (Anacker et al, 2014;Maccari, Krugers, Morley-Fletcher, Szyf, & Brunton, 2014;Palma-Gudiel et al, 2015;Tyrka et al, 2016).…”

“…Maternal-origin hormones are hypothesized to orchestrate offspring's tradeoffs between developmental priorities in relation to maternal resources or environmental conditions (Allen-Blevins, Sela, & . Elevated maternal GCs are associated with impaired offspring immune development, slower motor development, and less sociable temperament (reviewed in Lu et al, 2019). Offspring can use maternal GCs to guide their development in an adaptive way (e.g.…”

Considering the Microbiome in Stress-Related and Neurodevelopmental Trajectories to Schizophrenia

“…The short-term effects of maternal stress may act through adverse pregnancy outcomes, while the long-term effects on neurodevelopment may involve altered neonatal stress programming and gut dysbiosis ( 95 ). Maternal stress increases fetal and neonatal exposure to maternal cortisol, altering growth and behavior in humans and animal models (reviewed in 96 ). Stress also has well-documented effects on the microbiome, which may in turn alter inflammation and neurodevelopment in a developing neonate ( 62 , 97 – 103 ).…”

Early-Life Maternal Deprivation Predicts Stronger Sickness Behaviour and Reduced Immune Responses to Acute Endotoxaemia in a Pig Model

“…Adversity at an early age has the greatest impact on the individual's development in the perinatal, adolescent and puberty phases, when the developing brain is particularly vulnerable to the programming effects of stress [3]. During these critical phases, acute or chronic stress can trigger long-lasting or even permanent changes in the metabolism, central nervous system and immune system of young individuals [4,5]. Pigs (Sus scrofa domesticus) are an ideal model species for studying the programming effects of early-life adversity [6,7] because they share similarities in brain anatomy and neurodevelopment with humans [8,9] and their immune system resembles that of humans to a large extent in anatomy, function and gene expression [10][11][12].…”