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

Abstract

It is well established that circulating maternal stress hormones (glucocorticoids, GCs) can alter offspring phenotype. There is also a growing body of empirical work, within ecology and evolution, indicating that maternal GCs link the environment experienced by the mother during gestation with changes in offspring phenotype. These changes are considered to be adaptive if the maternal environment matches the offspring's environment and maladaptive if it does not. While these ideas are conceptually sound, we lack a testable framework that can be used to investigate the fitness costs and benefits of altered offspring phenotypes across relevant future environments. We present error management theory as the foundation for a framework that can be used to assess the adaptive potential of maternal stress hormones on offspring phenotype across relevant postnatal scenarios. To encourage rigorous testing of our framework, we provide field‐testable hypotheses regarding the potential adaptive role of maternal stress across a diverse array of taxa and life histories, as well as suggestions regarding how our framework might provide insight into past, present, and future research. This perspective provides an informed lens through which to design and interpret experiments on the effects of maternal stress, provides a framework for predicting and testing variation in maternal stress across and within taxa, and also highlights how rapid environmental change that induces maternal stress may lead to evolutionary traps.

Maternal stress alters the phenotype of the mother, her eggs and her offspring in a wild‐caught lizard

“…The concurrent effects of GC manipulations on maternal behaviour and egg GC levels and other aspects of egg composition suggest that direct and indirect exposure to maternal GCs likely mediated the observed changes to offspring phenotype. Although we did not test the outcomes of our documented phenotypic changes under different environmental conditions (sensu Sheriff et al., ), prior information about the adaptive significance of these traits suggests that they may better match offspring to specific environments (Parker & Andrews, ; Romero et al., ; Thawley & Langkilde, ). A better understanding of all (direct and indirect) consequences of maternal stress effects on offspring will help to illuminate the evolutionary potential and ecological consequences of maternal GCs for adapting an offspring to a changing environment.…”

“…The biomedical community has explored the relationship between elevated maternal GCs and offspring with regards to human health, with resulting phenotypic responses commonly characterized as negative side effects to elevated maternal stress (Meaney et al., ; Seckl & Meaney, ; Weinstock, ). An alternative, ecologically driven hypothesis suggests that exposure to maternal GCs in utero or in ovo may adaptively prepare offspring for their future environment (Meylan & Clobert, ; Sheriff, Dantzer, Love, & Orrock, ; Sheriff & Love, ). For example, offspring of GC‐treated mothers fled towards refuge in response to acute stress more often than those from control mothers in the common lizard Lacerta vivipara (De Fraipont, Clobert, John‐Alder, & Meylan, ).…”

“…The effect of maternal stress on offspring phenotype has been proposed to function primarily via direct effects of exposure of the developing embryo to maternally derived GCs (Sheriff et al., ). However, elevated maternal GC levels may also indirectly alter offspring phenotype via changes in maternal physiology, behaviour, thermoregulation, and/or hormone and nutrient allocation to developing embryos (Cottrell, Holmes, Livingstone, Kenyon, & Seckl, ; Meylan, Belliure, Clobert, & de Fraipont, ; Sheriff et al., ).…”

“…For example, offspring of GC-treated mothers fled towards refuge in response to acute stress more often than those from control mothers in the common lizard Lacerta vivipara (De Fraipont, Clobert, John-Alder, & Meylan, 2000). As such, the influence of elevated maternal GCs on offspring phenotype, which we define as maternal stress effects (sensu Sheriff et al, 2017), has been proposed as a factor influencing ecological and evolutionary processes (Meylan, Miles, & Clobert, 2012;Sheriff, 2015;Sheriff et al, 2018).…”

Advances in population ecology and species interactions in mammals

“…For instance, hungry animals may tolerate greater predation risk when foraging (Caro 2005;Stankowich and Blumstein 2005), and young animals often exhibit different dietary preferences than older animals as a result of different nutritional needs, differences in experience, and other factors (Galef and Giraldeau 2001;Newman 2007). Maternal effects (i.e., maternally generated transgenerational phenotypic plasticity) may influence offspring foraging behavior (Maestripieri and Mateo 2009;Sheriff et al 2018). For example, offspring born to mothers that experienced reduced food availability exhibit more fearful and less exploratory behavior than do offspring of mothers who experienced higher food availability; maternal diet typically has a positive effect on food selection by offspring, with a variety of species tending to consume foods consumed by their mothers (Maestripieri and Mateo 2009;Sheriff et al 2018).…”