Playing it safe; risk-induced trait responses increase survival in the face of predation.

Predation risk effects are impacts on prey caused by predators that do not include consumption. These can include changes in prey behaviour, physiology, and morphology (i.e. risk-induced trait responses), which can have consequences to individual fitness and population dynamics (i.e. non-consumptive effects). While these risk-induced trait responses (RITRs) can lower individual fitness as compared to prey not exposed to risk, they are assumed to increase fitness in the presence of predators. While much work has been built upon this assumption, most evidence occurs in consumptive experiments where the trait values of consumed prey are unknown. We have little evidence showing individuals with a greater magnitude of RITR have greater survival. Here, we tested the hypothesis that RITRs increase survival in the presence of predators, but come at a cost to growth. We tested this hypothesis using Nucella lapillus as prey and Carcinus maenas as a predator and including mussels as a basal resource in a two-phase mesocosm experimental set-up. In phase 1, Nucella were placed into either a control or risk treatment (exposure to non-lethal Carcinus) for 28 days and their behaviour and growth measured. In phase 2, a lethal Carcinus was added to all mesocosms (non-lethal crabs were removed), and survival was recorded for 15 days. At the treatment (group) level, we found that Nucella exposed to predation risk in phase 1 had significantly greater risk aversion behaviour (summed score of risky vs. safe behaviour) and significantly lower growth. In phase 2, we found that Nucella exposed to predation risk had greater survival. At the individual level (regardless of treatment), we found that Nucella with greater risk aversion scores in phase 1 had significantly higher survival in phase 2 when exposed to a lethal predator, but this came at a cost to their growth. This study provides some of the first empirical evidence, at both the group and individual level, testing a long-held assumption that predation risk-induced behavioural responses increase survival in the face of direct predation, but that these responses come at a cost to the prey. These results add to our growing understanding of the benefits of RITRs to individual fitness and non-consumptive effects generally.

Predator-induced transgenerational plasticity in animals: a meta-analysis.

There is growing evidence that the environment experienced by one generation can influence phenotypes in the next generation via transgenerational plasticity (TGP). One of the best-studied examples of TGP in animals is predator-induced transgenerational plasticity, whereby exposing parents to predation risk triggers changes in offspring phenotypes. Yet, there is a lack of general consensus synthesizing the predator-prey literature with existing theory pertaining to ecology and evolution of TGP. Here, we apply a meta-analysis to the sizable literature on predator-induced TGP (441 effect sizes from 29 species and 49 studies) to explore five hypotheses about the magnitude, form and direction of predator-induced TGP. Hypothesis #1: the strength of predator-induced TGP should vary with the number of predator cues. Hypothesis #2: the strength of predator-induced TGP should vary with reproductive mode. Hypothesis #3: the strength and direction of predator-induced TGP should vary among offspring phenotypic traits because some traits are more plastic than others. Hypothesis #4: the strength of predator-induced TGP should wane over ontogeny. Hypothesis #5: predator-induced TGP should generate adaptive phenotypes that should be more evident when offspring are themselves exposed to risk. We found strong evidence for predator-induced TGP overall, but no evidence that parental predator exposure causes offspring traits to change in a particular direction. Additionally, we found little evidence in support of any of the specific hypotheses. We infer that the failure to find consistent evidence reflects the heterogeneous nature of the phenomena, and the highly diverse experimental designs used to study it. Together, these findings set an agenda for future work in this area.

A skewed literature: Few studies evaluate the contribution of predation-risk effects to natural field patterns.

A narrative in ecology is that prey modify traits to reduce predation risk, and the trait modification has costs large enough to cause ensuing demographic, trophic and ecosystem consequences, with implications for conservation, management and agriculture. But ecology has a long history of emphasising that quantifying the importance of an ecological process ultimately requires evidence linking a process to unmanipulated field patterns. We suspected that such process-linked-to-pattern (PLP) studies were poorly represented in the predation risk literature, which conflicts with the confidence often given to the importance of risk effects. We reviewed 29 years of the ecological literature which revealed that there are well over 4000 articles on risk effects. Of those, 349 studies examined risk effects on prey fitness measures or abundance (i.e., non-consumptive effects) of which only 26 were PLP studies, while 275 studies examined effects on other interacting species (i.e., trait-mediated indirect effects) of which only 35 were PLP studies. PLP studies were narrowly focused taxonomically and included only three that examined unmanipulated patterns of prey abundance. Before concluding a widespread and influential role of predation-risk effects, more attention must be given to linking the process of risk effects to unmanipulated patterns observed across diverse ecosystems.

The influence of maternal glucocorticoids on offspring phenotype in high- and low-risk environments.

Elevated maternal glucocorticoid levels during gestation can lead to phenotypic changes in offspring via maternal effects. Although such effects have traditionally been considered maladaptive, maternally derived glucocorticoids may adaptively prepare offspring for their future environment depending upon the correlation between maternal and offspring environments. Nevertheless, relatively few studies test the effects of prenatal glucocorticoid exposure across multiple environments. We tested the potential for ecologically relevant increases in maternal glucocorticoids in the eastern fence lizard (Sceloporus undulatus) to induce adaptive phenotypic changes in offspring exposed to high or low densities of an invasive fire ant predator. Maternal treatment had limited effects on offspring morphology and behavior at hatching, but by 10 days of age, we found maternal treatment interacted with offspring environment to alter anti-predator behaviors. We did not detect differences in early-life survival based on maternal treatment or offspring environment. Opposing selection on anti-predator behaviors from historic and novel invasive predators may confound the potential of maternal glucocorticoids to adaptively influence offspring behavior. Our test of the phenotypic outcomes of transgenerational glucocorticoid effects across risk environments provides important insight into the context-specific nature of this phenomenon and the importance of understanding both current and historic evolutionary pressures.

Elevated glucocorticoids during gestation suggest sex-specific effects on offspring telomere lengths in a wild lizard.

The effects of maternal glucocorticoids (e.g. corticosterone, CORT) on offspring interest biologists due to increasing environmental perturbations. While little is known about the impact of maternal CORT on offspring fitness, it may modulate telomere length and compromise offspring health. Here, we use a modified real-time quantitative PCR assay to assess telomere length using small DNA quantities (<60 ng). We tested the hypothesis that increased maternal CORT during gestation decreases offspring telomere length. While CORT-driven telomere shortening is well established within individuals, cross-generational effects remain unclear. We treated wild-caught gravid female eastern fence lizards (Sceloporus undulatus) with daily transdermal applications of CORT, at ecologically relevant levels, from capture to laying. Maternal CORT treatment did not alter maternal telomere length, although baseline maternal CORT concentrations had a weak, negative correlation with maternal telomere length. There was no relation between mother and offspring telomere length. There was a trend for maternal CORT treatment to shorten telomeres of sons but not daughters. Our treatment replicated exposure to a single stressor per day, likely underestimating effects seen in the wild where stressors may be more frequent. Future research should further explore fitness consequences of maternal CORT effects.

Where and when to hunt? Decomposing predation success of an ambush carnivore.

Predator-prey games emerge when predators and prey dynamically respond to the behavior of one another, driving the outcomes of predator-prey interactions. Predation success is a function of the combined probabilities of encountering and capturing prey, which are influenced by both prey behavior and environmental features. While the relative importance of encounter and capture probabilities have been evaluated in a spatial framework, temporal variation in prey behavior and intrinsic catchability are likely to also affect the distribution of predation events. Using a single-predator-single-prey (puma-vicuña) system, we evaluated which factors predict predation events across both temporal and spatial dimensions of the components of predation by testing the prey-abundance hypothesis (predators select for high encounter probability) and the prey-catchability hypothesis (predators select for high relative capture probability) in time and space. We found that for both temporal and spatial analyses, neither the prey-abundance hypothesis nor the prey-catchability hypothesis alone predicted kill frequency or distribution; puma kill frequency was static throughout the diel cycle and pumas consistently selected a single habitat type when hunting, despite temporal and spatial variation in encounter rates and intrinsic catchability. Our integrated spatiotemporal analysis revealed that an interaction between time of day and habitat influences kill probability, suggesting that trade-offs in the temporal and spatial components of predation drive the probability of predation events. These findings reinforce the importance of examining both the temporal and spatial patterns of the components of predation, rather than unidimensional measures of predator or prey behavior, to comprehensively describe the feedbacks between predator and prey in the predator-prey game.

A framework and standardized terminology to facilitate the study of predation-risk effects.

The very presence of predators can strongly influence flexible prey traits such as behavior, morphology, life history, and physiology. In a rapidly growing body of literature representing diverse ecological systems, these trait (or "fear") responses have been shown to influence prey fitness components and density, and to have indirect effects on other species. However, this broad and exciting literature is burdened with inconsistent terminology that is likely hindering the development of inclusive frameworks and general advances in ecology. We examine the diverse terminology used in the literature, and discuss pros and cons of the many terms used. Common problems include the same term being used for different processes, and many different terms being used for the same process. To mitigate terminological barriers, we developed a conceptual framework that explicitly distinguishes the multiple predation-risk effects studied. These multiple effects, along with suggested standardized terminology, are risk-induced trait responses (i.e., effects on prey traits), interaction modifications (i.e., effects on prey-other-species interactions), nonconsumptive effects (i.e., effects on the fitness and density of the prey), and trait-mediated indirect effects (i.e., the effects on the fitness and density of other species). We apply the framework to three well studied systems to highlight how it can illuminate commonalities and differences among study systems. By clarifying and elucidating conceptually similar processes, the framework and standardized terminology can facilitate communication of insights and methodologies across systems and foster cross-disciplinary perspectives.

Proportional fitness loss and the timing of defensive investment: a cohesive framework across animals and plants.

The risk of consumption is a pervasive aspect of ecology and recent work has focused on synthesis of consumer-resource interactions (e.g., enemy-victim ecology). Despite this, theories pertaining to the timing and magnitude of defenses in animals and plants have largely developed independently. However, both animals and plants share the common dilemma of uncertainty of attack, can gather information from the environment to predict future attacks and alter their defensive investment accordingly. Here, we present a novel, unifying framework based on the way an organism's ability to defend itself during an attack can shape their pre-attack investment in defense. This framework provides a useful perspective on the nature of information use and variation in defensive investment across the sequence of attack-related events, both within and among species. It predicts that organisms with greater proportional fitness loss if attacked will gather and respond to risk information earlier in the attack sequence, while those that have lower proportional fitness loss may wait until attack is underway. This framework offers a common platform to compare and discuss consumer effects and provides novel insights into the way risk information can propagate through populations, communities, and ecosystems.

Validation of a noninvasive technique to quantify stress in northern bobwhite (Colinus virginianus).

Examination of the endocrine system through non-invasive fecal sampling may improve population management more than using demographic indicators alone. By addressing the physiological mechanisms that are influencing fitness, management actions can be proactively developed to alleviate stressors. Proactive determination of vulnerable populations is critical for species of concern, such as the Northern Bobwhite (Colinus virginianus), which have suffered decades of population decline. We validated an assay to noninvasively measure the adrenocortical response of captive reared bobwhite through fecal corticosterone metabolites (FCM). All individuals received three sequential 48-hour treatments in which samples were collected every 4 hours, including a reference period, an adrenocorticotropic hormone (ACTH) challenge and a biological stressor (exposure to a hunting dog). Reference FCM values had a mean concentration of 16.75 pg/mg (95% CrI: 13.68, 19.91) with adrenocortical activity increasing by 73% for the duration of the ACTH challenge (29.00 pg/mg; CrI: 25.01, 33.78). FCM concentrations remained similar to that of the reference levels during the biological stressor (16.56 pg/mg; CrI: 13.33, 19.92). Our study validates the use of feces to detect changes in FCM levels in our subject species but also demonstrates the complexity of FCM and the importance of both physiological and biological validation prior to field implementation.

Non-consumptive predator effects on prey population size: A dearth of evidence.

There is a large and growing interest in non-consumptive effects (NCEs) of predators. Diverse and extensive evidence shows that predation risk directly influences prey traits, such as behaviour, morphology and physiology, which in turn, may cause a reduction in prey fitness components (i.e. growth rate, survival and reproduction). An intuitive expectation is that NCEs that reduce prey fitness will extend to alter population growth rate and therefore population size. However, our intensive literature search yielded only 10 studies that examined how predator-induced changes in prey traits translate to changes in prey population size. Further, the scant evidence for risk-induced changes on prey population size have been generated from studies that were performed in very controlled systems (mesocosm and laboratory), which do not have the complexity and feedbacks of natural settings. Thus, although likely that predation risk alone can alter prey population size, there is little direct empirical evidence that demonstrates that it does. There are also clear reasons that risk effects on population size may be much smaller than the responses on phenotype and fitness components that are typically measured, magnifying the need to show, rather than infer, effects on population size. Herein we break down the process of how predation risk influences prey population size into a chain of events (predation risk affects prey traits, which affect prey fitness components and population growth rate, which affect prey population size), and highlight the complexity of each transition. We illustrate how the outcomes of these transitions are not straightforward, and how environmental context strongly dictates the direction and magnitude of effects. Indeed, the high variance in prey responses is reflected in the variance of results reported in the few studies that have empirically quantified risk effects on population size. It is therefore a major challenge to predict population effects given the complexity of how environmental context interacts with predation risk and prey responses. We highlight the critical need to appreciate risk effects at each level in the chain of events, and that changes at one level cannot be assumed to translate into changes in the next because of the interplay between risk, prey responses, and the environment. The gaps in knowledge we illuminate underscore the need for more evidence to substantiate the claim that predation risk effects extend to prey population size. The lacunae we identify should inspire future studies on the impact of predation risk on population-level responses in free-living animals.

Transgenerational Plasticity in Human-Altered Environments.

Our ability to predict how species will respond to human-induced rapid environmental change (HIREC) may depend upon our understanding of transgenerational plasticity (TGP), which occurs when environments experienced by previous generations influence phenotypes of subsequent generations. TGP evolved to help organisms cope with environmental stressors when parental environments are highly predictive of offspring environments. HIREC can alter conditions that favored TGP in historical environments by reducing parents' ability to detect environmental conditions, disrupting previous correlations between parental and offspring environments, and interfering with the transmission of parental cues to offspring. Because of the propensity to produce errors in these processes, TGP will likely generate negative fitness outcomes in response to HIREC, though beneficial fitness outcomes may occur in some cases.

Habitat complexity mediates the predator-prey space race.

The spatial relationship between predator and prey is often conceptualized as a behavioral response race, in which prey avoid predators while predators track prey. Limiting habitat types can create spatial anchors for prey or predators, influencing the likelihood that the predator or prey response will dominate. Joint spatial anchors emerge when predator and prey occupy similar feeding habitat domains and risk and reward become spatially conflated, confusing predictions of which player will win the space race. These spatial dynamics of risk-foraging trade-offs are often obscured by habitat heterogeneity and community complexity in large vertebrate systems, fueling ambiguity regarding the generality of predictions from predator-prey theory. To test how habitat distribution influences the predator-prey space race, we examine correlation in puma and vicuña habitat selection and space use at two sites, one of which generates a distinct risk-foraging trade-off at a joint spatial anchor. The distribution of vegetation, which serves as both forage for vicuñas and stalking cover for pumas, differs between the sites; the llano contains a single central meadow that acts as a joint spatial anchor, while the canyon is characterized by more heterogeneous vegetation. Puma-vicuña habitat selection correlation was positive in the llano and negative in the canyon, and similarly, utilization distributions were more strongly correlated in the llano than the canyon. Vicuña locations occurred at higher values of puma habitat selection and utilization in the llano than in the canyon. Similarly, puma locations in the llano occurred at higher values of vicuña habitat selection and utilization than in the canyon. Although pumas consistently selected for and utilized vegetative and topographic cover regardless of habitat distribution, vicuñas only selected against vegetation in the heterogeneous canyon site, reducing spatial correlation with pumas. Our work suggests a joint spatial anchor favors pumas in the space race due to the inability for vicuñas to avoid crucial foraging habitat. The outcome of the predator-prey space race appears to be strongly informed by the distribution of habitat, whereby corresponding predictability of predator and prey favors predators in the spatial game.

Maternal corticosterone increases thermal sensitivity of heart rate in lizard embryos.

While it is well established that maternal stress hormones, such as corticosterone (CORT), can induce transgenerational phenotypic plasticity, few studies have addressed the influence of maternal CORT on pre-natal life stages. We tested the hypothesis that experimentally increased CORT levels of gravid female eastern fence lizards ( Sceloporus undulatus) would alter within-egg embryonic phenotype, particularly heart rates. We found that embryos from CORT-treated mothers had heart rates that increased faster with increasing temperature, resulting in higher heart rates at developmentally relevant temperatures but similar heart rates at maintenance relevant temperatures, compared with embryos of control mothers. Thus, maternal CORT appears to alter the physiology of pre-natal offspring. This may speed development and decrease the amount of time spent in eggs, the most vulnerable stage of life.

Integrating temporal refugia into landscapes of fear: prey exploit predator downtimes to forage in risky places.

The landscape of fear is an important driver of prey space use. However, prey can navigate the landscape of fear by exploiting temporal refuges from predation risk. We hypothesized that diel patterns of predator and prey movement and space use would be inversely correlated due to temporal constraints on predator habitat domain. Specifically, we evaluated habitat selection and activity of the vicuña and its only predator, the puma, during three diel periods: day, dawn/dusk, and night. Pumas selected the same habitats regardless of diel period-vegetated and rugged areas that feature stalking cover for pumas-but increased their activity levels during dawn/dusk and night when they benefit from reduced detection by prey. Vicuñas avoided areas selected by pumas and reduced activity at night, but selected vegetated areas and increased activity by day and dawn/dusk. Vicuña habitat selection and movement strategies appeared to reduce the risk of encountering pumas; movement rates of pumas and vicuñas were negatively correlated across the diel cycle, and habitat selection was negatively correlated during dawn/dusk and night. Our study shows that an ambush predator's temporal activity and space use patterns interact to create diel refugia and shape the antipredator behaviors of its prey. Importantly, it is likely the very nature of ambush predators' static habitat specificity that makes predator activity important to temporally varying perceptions of risk. Prey which depend on risky habitats for foraging appear to mitigate risk by feeding when they can more easily detect predators and when predators are least active.

Snow roosting reduces temperature-associated stress in a wintering bird.

Animals in temperate northern regions employ a variety of strategies to cope with the energetic demands of winter. Behavioral plasticity may be important, as winter weather conditions are increasingly variable as a result of modern climate change. If behavioral strategies for thermoregulation are no longer effective in a changing environment, animals may experience physiological stress, which can have fitness consequences. We monitored winter roosting behavior of radio-tagged ruffed grouse (Bonasa umbellus), recorded snow depth and temperature, and assayed droppings for fecal corticosterone metabolites (FCM). Grouse FCM levels increased with declining temperatures. FCM levels were high when snow was shallow, but decreased rapidly as snow depth increased beyond 20 cm. When grouse used snow burrows, there was no effect of temperature on FCM levels. Snow burrowing is an important strategy that appears to allow grouse to mediate the possibly stressful effects of cold temperatures. This is one of the first studies to explore how variable winter weather conditions influence stress in a free-living cold-adapted vertebrate and its ability to mediate this relationship behaviorally. Animals that depend on the snowpack as a winter refuge will likely experience increased stress and possible fitness costs resulting from the loss of snow cover due to climate change.

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

While biomedical researchers have long appreciated the influence of maternally derived glucocorticoids (GCs) on offspring phenotype, ecologists have only recently begun exploring its impact in wild animals. Interpreting biomedical findings within an ecological context has posited that maternal stress, mediated by elevations of maternal GCs, may play an adaptive role preparing offspring for a stressful or rigorous environment. Yet, the influence of maternal stress on offspring phenotype has been little studied in wild animals. We experimentally elevated GCs to ecologically relevant levels (mimicking increases in maternal stress hormones following a nonlethal predator encounter, a heat challenge, or a chasing or confinement stressor) in female eastern fence lizards Sceloporus undulatus during gestation. We tested the hypothesis that maternally derived stress hormones themselves are sufficient to alter offspring phenotype. Specifically, we examined the effects of experimentally elevated maternal GCs on fitness-relevant traits of the mother, her eggs and her subsequent offspring. We found that daily maternal GC elevation: (a) increased maternal antipredator behaviours and postlaying glucose levels; (b) had no effect on egg morphology or caloric value, but altered yolk hormone (elevated GC) and nutrient content; and (c) altered offspring phenotype including stress-relevant physiology, morphology and behaviour. These findings reveal that maternally derived GCs alone can alter offspring phenotype in a wild animal, changes that may be mediated via maternal behaviour, and egg hormone and nutrient content. Understanding the ecological consequences of these effects under different environmental conditions will be critical for determining the adaptive significance of elevated maternal GCs for offspring.

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

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.

Coping with differences in snow cover: the impact on the condition, physiology and fitness of an arctic hibernator.

The Earth's climate is changing at an unprecedented rate and, as ecologists, we are challenged with the difficult task of predicting how individuals and populations will respond to climate-induced changes to local and global ecosystems. Although we are beginning to understand some of the responses to changing seasonality, the physiological mechanisms that may drive these responses remain unknown. Using long-term data comparing two nearby populations (<20 km apart) of free-living arctic ground squirrels in northern Alaska, we have previously shown that the timing of spring snowmelt greatly influences their phenology of hibernation and reproduction in a population and site-specific manner. Here, we integrate these site-specific phenologies with body condition, stress physiology, reproductive success and juvenile recruitment to understand phenotypic selection in the two populations. We found that at the site with relatively late spring snowmelt and early autumn snow cover: (i) adult females were larger and in better body condition but had significantly higher stress hormone levels; (ii) females had similar numbers of comparably sized offspring, but offspring had higher stress hormone levels; and (iii) offspring density was lower just prior to hibernation. Thus, adult females at the two sites appear to use different coping strategies that allow them to maintain reproductive fitness; however, marked shortening of the active season because of later snowmelt in spring and earlier snow cover in autumn may compromise juvenile recruitment. We discuss the significance of these findings within the broader context of changing animal-environment relationships.

Sex-Dependent Phenological Plasticity in an Arctic Hibernator.

Hibernation provides a means of escaping the metabolic challenges associated with seasonality, yet the ability of mammals to prolong or reenter seasonal dormancy in response to extreme weather events is unclear. Here, we show that Arctic ground squirrels in northern Alaska exhibited sex-dependent plasticity in the physiology and phenology of hibernation in response to a series of late spring snowstorms in 2013 that resulted in the latest snowmelt on record. Females and nonreproductive males responded to the >1-month delay in snowmelt by extending heterothermy or reentering hibernation after several days of euthermy, leading to a >2-week delay in reproduction compared to surrounding years. In contrast, reproductive males neither extended nor reentered hibernation, likely because seasonal gonadal growth and development and subsequent testosterone release prevents a return to torpor. Our findings reveal intriguing differences in responses of males and females to climatic stressors, which can generate a phenological mismatch between the sexes.

Integrating Ecological and Evolutionary Context in the Study of Maternal Stress.

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.