Maternal adversity and ecological stressors in natural populations: the role of stress axis programming in individuals, with implications for populations and communities

Biomedical researchers have long appreciated that maternal stressors can induce preparative and adaptive programming in offspring via exposure to maternal Glucocorticoids (GCs). However, few ecologists are aware of the capacity for maternal GC exposure to translate ecological and environmental stressors into preparative and adaptive programmed offspring responses in free-living systems. We review a growing body of experimental work indicating that circulating maternal GCs link ecological stressors with adaptive programming of the stress axis. Throughout, we emphasise that natural and human-induced ecological stressors play a fundamental role in programming the capacity of individuals, populations and communities to respond to both predictable and unpredictable ecological change via translating maternal adversity into responsive programming of the vertebrate stress axis. To encourage rigorous testing of this paradigm in a broad range of ecological systems, we introduce the principal extrinsic stressors with a recognised potential to alter maternal circulating GC levels. We then review from the biomedical literature regarding the underlying physiological and epigenetic mechanisms of stress-induced programming of individual phenotypes to predict how variation in ecological stressors can produce individual variation in stress axis management. To appreciate the potential evolutionary inertia (i.e. adaptive value) of maternally programmed individual variation, we review key recent studies in free-living systems that test its adaptive function, and then discuss how variation in stress-axis programming may scale up to influence populations and ecological communities. Given the huge potential of this field, it is encouraging that ecologists are beginning to examine how and why maternal GCs translate ecological and environmental stressors into preparative stress axis programming in free-living systems.