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

Abstract

Summary1. 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. 2. 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. 3. 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. 4. 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.

Programming of the hypothalamic-pituitary-interrenal axis by maternal social status in zebrafish (Danio rerio)

“…Although few studies have assessed HPI responsiveness in fish as a result of maternal stress, studies on avian and mammalian species are more abundant (reviewed by Love et al, 2013). Maternal programming of hypothalamic-pituitary-adrenal (HPA) axis responsiveness in mammals has been well studied for both the prenatal (by maternal stress, e.g.…”

Developmental stress increases reproductive success in male zebra finches

“…Although many of the phenotypic consequences of developmental stress appear overwhelmingly negative, there is increasing evidence for an adaptive function of developmental stress (reviewed in [65][66][67][68][69]). For example, stress exposure during development may induce phenotypic changes which prepare developing animals to live in harsh environments or match offspring needs to parental capabilities [8,56,66].…”

Error management theory and the adaptive significance of transgenerational maternal‐stress effects on offspring phenotype

“…To move this field ahead in a productive manner, we suggest that three critical points must be considered prior to assigning any hypothetical adaptive or maladaptive value to maternal‐stress effects ( sensu Love et al., 2013; Sheriff & Love, 2013; Uller et al., 2013; Sheriff et al., 2017). First, we must appreciate that the value of any phenotype, whether stress‐induced or not, can only be understood by examining performance or fitness in an ecologically relevant context (and not simply assuming the outcome based on the phenotype alone).…”

“…Recently, this phenomenon has been increasingly studied in vertebrates in the context of maternal‐stress effects, largely because the maternal phenotype or cue that may induce plasticity in offspring traits (maternal stress hormone levels) is both measurable and amenable to experimental manipulations. In vertebrates, exposure to maternally derived stress hormones (glucocorticoids; i.e., “maternal stress”) is increasingly recognized as a significant factor mediating transgenerational phenotypic plasticity in offspring (Barbazanges, Piazza, Moal, & Maccari, 1996; Gluckman, Hanson, & Spencer, 2005; Love, McGowan, & Sheriff, 2013; Meaney, Szyf, & Seckl, 2007). The consequences of maternal stress have long been considered to be maladaptive in biomedical fields because offspring phenotypes that can occur in response to maternal stress (e.g., smaller size, slower growth, lower energetic demand, higher anxiety‐like behavior) are assumed to confer reduced fitness (Sheriff & Love, 2013).…”