Multiple Environmental Stressors Induce an Adaptive Maternal Effect

Abstract

Evolution of adaptation requires predictability and recurrence of functional contexts. Yet organisms live in multifaceted environments that are dynamic and ever changing, making it difficult to understand how complex adaptations evolve. This problem is particularly apparent in the evolution of adaptive maternal effects, which are often assumed to require reliable and discrete cues that predict conditions in the offspring environment. One resolution to this problem is if adaptive maternal effects evolve through preexisting, generalized maternal pathways that respond to many cues and also influence offspring development. Here, we assess whether an adaptive maternal effect in western bluebirds is influenced by maternal stress pathways across multiple challenging environments. Combining 18 years of hormone sampling across diverse environmental contexts with an experimental manipulation of the competitive environment, we show that multiple environmental factors influenced maternal corticosterone levels, which, in turn, influenced a maternal effect on aggression of sons in adulthood. Together, these results support the idea that multiple stressors can induce a known maternal effect in this system. More generally, they suggest that activation of general pathways, such as the hypothalamic-pituitary-adrenal axis, may simplify and facilitate the evolution of adaptive maternal effects by integrating variable environmental conditions into preexisting maternal physiological systems.