Stress in the social context: a behavioural and eco-evolutionary perspective.

The social environment is one of the primary sources of challenging stimuli that can induce a stress response in animals. It comprises both short-term and stable interactions among conspecifics (including unrelated individuals, mates, potential mates and kin). Social stress is of unique interest in the field of stress research because (1) the social domain is arguably the most complex and fluctuating component of an animal's environment; (2) stress is socially transmissible; and (3) stress can be buffered by social partners. Thus, social interactions can be both the cause and cure of stress. Here, we review the history of social stress research, and discuss social stressors and their effects on organisms across early life and adulthood. We also consider cross-generational effects. We discuss the physiological mechanisms underpinning social stressors and stress responses, as well as the potential adaptive value of responses to social stressors. Finally, we identify outstanding challenges in social stress research, and propose a framework for addressing these in future work.

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 quantitative synthesis of and predictive framework for studying winter warming effects in reptiles.

Increases in temperature related to global warming have important implications for organismal fitness. For ectotherms inhabiting temperate regions, 'winter warming' is likely to be a key source of the thermal variation experienced in future years. Studies focusing on the active season predict largely positive responses to warming in the reptiles; however, overlooking potentially deleterious consequences of warming during the inactive season could lead to biased assessments of climate change vulnerability. Here, we review the overwinter ecology of reptiles, and test specific predictions about the effects of warming winters, by performing a meta-analysis of all studies testing winter warming effects on reptile traits to date. We collated information from observational studies measuring responses to natural variation in temperature in more than one winter season, and experimental studies which manipulated ambient temperature during the winter season. Available evidence supports that most reptiles will advance phenologies with rising winter temperatures, which could positively affect fitness by prolonging the active season although effects of these shifts are poorly understood. Conversely, evidence for shifts in survivorship and body condition in response to warming winters was equivocal, with disruptions to biological rhythms potentially leading to unforeseen fitness ramifications. Our results suggest that the effects of warming winters on reptile species are likely to be important but highlight the need for more data and greater integration of experimental and observational approaches. To improve future understanding, we recap major knowledge gaps in the published literature of winter warming effects in reptiles and outline a framework for future research.

Context-dependent effects of glucocorticoids on the lizard gut microbiome.

The vertebrate gut microbiota (bacterial, archaeal and fungal communities of the gastrointestinal tract) can have profound effects on the physiological processes of their hosts. Although relatively stable, changes in microbiome structure and composition occur due to changes in the environment, including exposure to stressors and associated increases in glucocorticoid hormones. Although a growing number of studies have linked stressor exposure to microbiome changes, few studies have experimentally explored the specific influence of glucocorticoids on the microbiome in wild animals, or across ecologically important processes (e.g., reproductive stages). Here we tested the response of the gut microbiota of adult female Sceloporus undulatus across gestation to ecologically relevant elevations of a stress-relevant glucocorticoid hormone (CORT) in order to determine (i) how experimentally elevated CORT influenced microbiome characteristics, and (ii) whether this relationship was dependent on reproductive context (i.e., whether females were gravid or not, and, in those that were gravid, gestational stage). We show that the effects of CORT on gut microbiota are complex and depend on both gestational state and stage. CORT treatment altered microbial community membership and resulted in an increase in microbiome diversity in late-gestation females, and microbial community membership varied according to treatment. In nongravid females, CORT treatment decreased interindividual variation in microbial communities, but this effect was not observed in late-gestation females. Our results highlight the need for a more holistic understanding of the downstream physiological effects of glucocorticoids, as well as the importance of context (here, gestational state and stage) in interpreting stress effects in ecology.

Viviparous mothers impose stronger glucocorticoid-mediated maternal stress effects on their offspring than oviparous mothers.

Maternal stress during gestation has the potential to affect offspring development via changes in maternal physiology, such as increases in circulating levels of glucocorticoid hormones that are typical after exposure to a stressor. While the effects of elevated maternal glucocorticoids on offspring phenotype (i.e., "glucocorticoid-mediated maternal effects") have been relatively well established in laboratory studies, it remains poorly understood how strong and consistent such effects are in natural populations. Using a meta-analysis of studies of wild mammals, birds, and reptiles, we investigate the evidence for effects of elevated maternal glucocorticoids on offspring phenotype and investigate key moderators that might influence the strength and direction of these effects. In particular, we investigate the potential importance of reproductive mode (viviparity vs. oviparity). We show that glucocorticoid-mediated maternal effects are stronger, and likely more deleterious, in mammals and viviparous squamate reptiles compared with birds, turtles, and oviparous squamates. No other moderators (timing and type of manipulation, age at offspring measurement, or type of trait measured) were significant predictors of the strength or direction of the phenotypic effects on offspring. These results provide evidence that the evolution of a prolonged physiological association between embryo and mother sets the stage for maladaptive, or adaptive, prenatal stress effects in vertebrates driven by glucocorticoid elevation.

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.

Academic ecosystems must evolve to support a sustainable postdoc workforce.

The postdoctoral workforce comprises a growing proportion of the science, technology, engineering and mathematics (STEM) community, and plays a vital role in advancing science. Postdoc professional development, however, remains rooted in outdated realities. We propose enhancements to postdoc-centred policies and practices to better align this career stage with contemporary job markets and work life. By facilitating productivity, wellness and career advancement, the proposed changes will benefit all stakeholders in postdoc success-including research teams, institutions, professional societies and the scientific community as a whole. To catalyse reform, we outline recommendations for (1) skills-based training tailored to the current career landscape, and (2) supportive policies and tools outlined in postdoc handbooks. We also invite the ecology and evolution community to lead further progressive reform.

Gestation alters the gut microbiota of an oviparous lizard.

Mammalian pregnancy can alter the diversity, membership and structure of the maternal gut microbiota, but it is unclear whether this phenomenon occurs in vertebrates with different reproductive strategies. We conducted 16S rRNA bacterial inventories to investigate whether oviparous lizards exhibit shifts in gut microbiota similar to those observed in mammals. Using wild-caught eastern fence lizards from Alabama, USA, we collected and extracted fecal DNA from gravid and non-gravid individuals over 54 days in captivity. We predicted that, like mammals, the alpha diversity of lizard gut microbiota would decrease over gestation, and that inter-individual variation in community composition would increase. Indeed, we found that individuals in late-gestation harbored lower gut bacterial richness compared to non-gravid females. Lizard gut microbial communities of late-gestational females exhibited higher pairwise distances for both community membership and community structure compared to earlier gestation stages, indicating a higher degree of inter-individual variation as gestation progressed. Additionally, we found that the relative abundance and prevalence of the candidate phylum Melainabacteria tended to decrease over the course of gestation. While the consequences of these specific alterations are unknown, our results suggest that a general restructuring of gut microbial communities over gestation may be widespread across vertebrate reproductive strategies.

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.

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.

In ovo microbial communities: a potential mechanism for the initial acquisition of gut microbiota among oviparous birds and lizards.

Vertebrate gut microbiota mediate critical physiological processes known to affect host fitness, but the mechanisms that expose wildlife to pioneer members of this important microbial community are not well understood. For example, oviparous vertebrates are thought to acquire gut microbiota through post-natal exposure to the external environment, but recent evidence from placental mammals suggests that the vertebrate reproductive tract harbours microbiota that may inoculate offspring in utero These findings suggest that oviparous vertebrates may be capable of acquiring pioneer microbiota in ovo, but this phenomenon remains unexplored. To fill this knowledge gap, we used culture-independent inventories to determine if the eggs of wild birds and lizards harboured in ovo microbial communities. Our approach revealed distinct in ovo bacterial communities, but fungal communities were indistinguishable from controls. Further, lizard eggs from the same clutch had bacterial community structures that were more similar to each other than to unrelated individuals. These results suggest that oviparous vertebrates may acquire maternal microbiota in ovo, possibly through the inoculation of egg yolk prior to shelling. Therefore, this study may provide a first glimpse of a phenomenon with substantial implications for our understanding of the ecological and evolutionary factors shaping gut microbial communities.

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.

No apparent benefits of allonursing for recipient offspring and mothers in the cooperatively breeding meerkat.

Cooperative behaviours by definition are those that provide some benefit to another individual. Allonursing, the nursing of non-descendent young, is often considered a cooperative behaviour and is assumed to provide benefits to recipient offspring in terms of growth and survival, and to their mothers, by enabling them to share the lactation load. However, these proposed benefits are not well understood, in part because maternal and litter traits and other ecological and social variables are not independent of one another, making patterns hard to discern using standard univariate analyses. Here, we investigate the potential benefits of allonursing in the cooperatively breeding Kalahari meerkat, where socially subordinate females allonurse the young of a dominant pair without having young of their own. We use structural equation modelling to allow us to account for the interdependence of maternal traits, litter traits and environmental factors. We find no evidence that allonursing provides benefits to pups or mothers. Pups that received allonursing were not heavier at emergence and did not have a higher survival rate than pups that did not receive allonursing. Mothers whose litters were allonursed were not in better physical condition, did not reconceive faster and did not reduce their own nursing investment compared to mothers who nursed their litters alone. These patterns were not significantly influenced by whether mothers were in relatively good, or poor, condition. We suggest that allonursing may persist in this species because the costs to allonurses may be low. Alternatively, allonursing may confer other, more cryptic, benefits to pups or allonurses, such as immunological or social benefits.