Dr Michael Sheriff outlines how maternal stress effects may have evolved and explains seemingly maladaptive offspring responses.
Changes in the maternal phenotype can act as a signal to offspring about the future environment that they will encounter, and these cues can induce adaptive response in offspring phenotypes (e.g., behaviour, morphology, physiology). This phenomenon has been increasingly studied in animals in the context of maternal-stress effects, largely because maternal stress hormones that may induce changes in offspring traits is both measureable and amenable to experimental manipulations.
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., small size, slow growth, anxiety-like behaviour) are assumed to confer reduced fitness. However, researchers have recently proposed that maternal stress can play adaptive roles across a wide variety of animal taxa if stress-induced phenotypes better prepare offspring for a stressful post-natal environment.
Despite this recent progress, there remains much controversy, particularly given that animals still seemingly have maladaptive responses (e.g., in lab rodents, a single stressful exposure during gestation results in a significant change in offspring traits in an otherwise benign lifetime environment). I, along with colleagues, have proposed a unified framework that both explains the selective mechanisms and allows field-testing of the adaptive role of maternal stress. This framework helps to explain seemingly maladaptive maternal-stress induced trait changes in offspring.
The adaptive potential of maternal stress
The ecology of maternal stress has been an active area of recent research, yet the traditional biomedical view that maternal stress generates negative outcomes for both mothers and offspring (i.e., is maladaptive) often still prevails. To move this field ahead in a productive manner, three critical points must be considered prior to assigning any hypothetical adaptive or maladaptive value to maternal-stress effects:
- A phenotype does not have an inherent value, and can only be understood by examining performance or fitness in an ecologically-relevant context;
- The evolutionary and life-history context of the organism must be understood before experiments can be designed to test phenotype-performance relationships. For example, if predation risk is the most salient selection pressure in the evolution of a species’ stress response, testing phenotypic performance in a food-restricted environment is unlikely to yield useful inference regarding the fitness value of stress-mediated offspring plasticity; and
- Testing phenotypic performance in a singular, benign post-natal environment is invalid for determining the adaptive potential of maternal stress. Offspring performance must be tested in both a stressful and benign environment. Stated another way, the fitness outcomes of offspring phenotypes induced by elevated maternal stress need to be examined across more biologically and ecologically appropriate environments.
Maternal stress in nature
In nature, animals interact with their environments over dynamic spatio-temporal scales. 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.
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 (see Fig. 1). Importantly, there are likely very different costs/benefits associated with offspring phenotypic performance depending upon the match or mismatch to future environments, and the costs of mismatches, not matches, are expected to play a significant role in the origin and maintenance of transgenerational maternal-stress effects.
Using error management theory to understand maternal-stress effects
Error management theory (EMT) is an evolutionary perspective that provides a formal theoretical framework for evaluating how organisms (including humans) should make decisions amidst uncertainty. It theorises that when decision errors have different fitness costs (or benefits), selection will favour individuals that err towards making the least costly error to avoid making a costlier one. For example, your smoke detector in your house is sensitive enough to often alarm when you have simply burnt toast, an error designed to avoid the much more costly error of the alarm not going off when the house is actually on fire.
EMT can be used to assess whether the effects of maternal stress on offspring phenotype generate relatively better (benefits) or worse (costs) fitness outcomes for mothers or offspring depending on the relative match of the adjusted offspring phenotype to the future environment (see Fig. 1). Because future conditions cannot be predicted with complete accuracy, there are four possible scenarios or outcomes:
- Unaltered offspring phenotype in a benign postnatal environment (no error);
- Altered offspring phenotype in a benign environment (error of unnecessary offspring modification);
- Unaltered offspring phenotype in a stressful environment (error of failing to modify offspring when necessary); and
- Altered offspring phenotype in a stressful environment (no error).
Although EMT typically focuses on the costs and benefits of errors in affecting optimal decision making, within the maternal stress framework, it is the costs and benefits of the actual decisions that are ultimately important and which influence the evolution of maternal-stress effects. In other words, it is critical to compare the relative fitness outcomes of unaltered against altered offspring phenotypes across all scenarios in a 2×2 manner.
Outstanding questions in integrating error management into maternal stress
To test the adaptive potential of maternal stress and tackle the complex relationship between maternal stress and offspring phenotype, my research group uses an interdisciplinary approach that combines the fields of physiology, ecology, neurobiology, and evolution. My work occurs both in the field and laboratory, almost exclusively with wild animals. Although I have worked for over a decade on understanding maternal stress from an ecological and evolutionary perspective, there still remains many outstanding questions in this relatively new field:
- Are the fitness benefits of maternal stress dependent upon the environment offspring experience at independence? We must consider this across ecologically relevant environments;
- Are the effects of maternal stress on offspring characteristics dependent upon the ecological trigger inducing maternal stress? Mothers may experience nutritional, predation, or climate-induced stress effects – does this alter the offspring phenotype differently?
- Do offspring or mothers control the point at which elevated maternal glucocorticoids alter offspring traits? Offspring and mothers can be in conflict with how maternal stress alters offspring traits, can offspring resist the effects of maternal glucocorticoids and, if so, how?
- What role do fathers play in this EMT view of maternal-stress effects? And
- How does anthropogenic environmental change modify the occurrence of errors in the maternal stress – offspring phenotype relationship? For example, the mismatch between maternal and offspring environments is likely elevated due to human-induced rapid environmental change, which should increase the frequency of errors.
Dr Michael J Sheriff
Department of Ecosystem Science and Management
College of Agricultural Sciences
Pennsylvania State University