Integrating Ecological and Evolutionary Context in the Study of Maternal Stress

Abstract

Maternal stress can prenatally influence offspring phenotypes and there are an increasing number of ecological studies that are bringing to bear biomedical findings to natural systems. This is resulting in a shift from the perspective that maternal stress is unanimously costly, to one in which maternal stress may be beneficial to offspring. However, this adaptive perspective is in its infancy with much progress to still be made in understanding the role of maternal stress in natural systems. Our aim is to emphasize the importance of the ecological and evolutionary context within which adaptive hypotheses of maternal stress can be evaluated. We present five primary research areas where we think future research can make substantial progress: (1) understanding maternal and offspring control mechanisms that modulate exposure between maternal stress and subsequent offspring phenotype response; (2) understanding the dynamic nature of the interaction between mothers and their environment; (3) integrating offspring phenotypic responses and measuring both maternal and offspring fitness outcomes under real-life (either free-living or semi-natural) conditions; (4) empirically testing these fitness outcomes across relevant spatial and temporal environmental contexts (both pre- and post-natal environments); (5) examining the role of maternal stress effects in human-altered environments-i.e., do they limit or enhance fitness. To make progress, it is critical to understand the role of maternal stress in an ecological context and to do that, we must integrate across physiology, behavior, genetics, and evolution.

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).…”

“…As such, the quality of the maternal and offspring environment may be temporally or spatially matched, such as may occur in species where there are overlapping generations (temporal matching) or where offspring disperse to areas that are similar to parental environments. Alternatively, past cues may not reliably predict the future (such as in long‐lived animals or those with long‐distance natal dispersal), increasing or decreasing the likelihood that the maternal and offspring environments match (Sheriff & Love, 2013; Sheriff et al., 2017). Thus, to correctly assess the potential adaptive role (if any) of maternal stress, the relative offspring phenotype fitness value across biologically relevant environmental scenarios must be examined (Figure 1; Love & Williams, 2008; Uller et al., 2013).…”

Sex‐dependent effects of maternal stress: Stressed moms invest less in sons than daughters

“…The mechanisms underlying sex‐specific maternal investment are poorly understood (Veller, Haig, & Nowak, ); however, maternal stress hormones (glucocorticoids; maternal CORT hereafter) may be one factor driving sex‐dependent maternal effects (Sheriff et al., ). Maternal CORT is directly related to the environment experienced by the mother, such as predation risk, food availability, and competition, and has been shown to reduce maternal investment in offspring (Thierry, Massemin, Handrich, & Raclot, ) and mediate offspring phenotype (reviewed in Saino, Romano, Ferrari, Martinelli, & Møller, ; Sheriff & Love, ).…”

Pre‐ and postnatal effects of experimentally manipulated maternal corticosterone on growth, stress reactivity and survival of nestling house wrens

“…If adverse conditions lead to an increase in maternal corticosterone during egg formation, and this increased corticosterone is transferred, at least to an extent, to the egg, the collateral damage hypothesis proposes that there will be long‐term, negative effects on offspring. In contrast, the environmental‐/maternal‐matching hypothesis posits that transfer of maternal corticosterone to the egg prepares offspring for the stressful environment that they are about to encounter, and is generally beneficial to offspring provided the maternal environment matches the offspring environment (Bonier, Moore, et al., ; Sheriff et al., ). Our results appear to be broadly consistent with the environmental‐/maternal‐matching hypothesis.…”

“…Negative correlations between corticosterone levels and body condition or habitat quality are consistent with this hypothesis (Jenni‐Eiermann et al., ; Müller et al., ), as are reports of negative effects of maternally derived corticosterone on nestling growth and development (Henriksen et al., ; Schoech et al., ). In contrast to this traditional view, an emerging body of empirical research suggests that maternal effects can be a powerful tool by which mothers shape the phenotype of their offspring so that they are optimally suited to the environment in which they develop, the environmental‐/maternal‐matching hypothesis (Crino & Breuner, ; Grindstaff, ; Henriksen et al., ; Merrill & Grindstaff, ; Sheriff & Love, ; Sheriff et al., ). This hypothesis posits a positive relationship between an increase in maternally derived corticosterone and offspring fitness, particularly if the corticosterone that females transfer to their offspring via the egg prepares offspring for success under the stressful conditions that their mother experienced (Chin et al., ; Groothuis, Müller, von Engelhardt, Carere, & Eising, ).…”