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\u27s 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

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.This article provides a quantitative framework as a means of generating field‐testable hypotheses regarding the adaptive potential of maternal stress under different scenario combinations. By providing a mechanistic basis for examining the adaptive potential of maternal stress effects, our overall aim is not only to provide a means for explaining patterns and testing new hypotheses, but to catalyze the study of maternal stress effects under this framework across a diversity of species, life histories, and environments.Peer Reviewedhttps://deepblue.lib.umich.edu/bitstream/2027.42/145404/1/ece34074_am.pdfhttps://deepblue.lib.umich.edu/bitstream/2027.42/145404/2/ece34074.pd

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\u27s 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

The Neurological Ecology of Fear: Insights Neuroscientists and Ecologists Have to Offer one Another

That the fear and stress of life-threatening experiences can leave an indelible trace on the brain is most clearly exemplified by post-traumatic stress disorder (PTSD). Many researchers studying the animal model of PTSD have adopted utilizing exposure to a predator as a life-threatening psychological stressor, to emulate the experience in humans, and the resulting body of literature has demonstrated numerous long-lasting neurological effects paralleling those in PTSD patients. Even though much more extreme, predator-induced fear and stress in animals in the wild was, until the 1990s, not thought to have any lasting effects, whereas recent experiments have demonstrated that the effects on free-living animals are sufficiently long-lasting to even affect reproduction, though the lasting neurological effects remain unexplored. We suggest neuroscientists and ecologists both have much to gain from collaborating in studying the neurological effects of predator-induced fear and stress in animals in the wild. We outline the approaches taken in the lab that appear most readily translatable to the field, and detail the advantages that studying animals in the wild can offer researchers investigating the “predator model of PTSD.

Equipped for Life in the Boreal Forest: The Role of the Stress Axis in Mammals

The hypothalamic-pituitary-adrenal axis (stress axis) plays a central role in equipping mammals to succeed in the challenging environment of the boreal forest. Over the last 20 years, we have tackled a broad range of topics to understand how the stress axis functions in four key herbivore species. The central challenge for snowshoe hares is coping with their predators, whereas for the others, it is primarily coping with each other (especially during reproduction) and with their physical environment. Hares are severely stressed by their predators during the population decline. The predator threat causes major changes in the stress axis of hares and reduces their reproduction; in addition, acting through maternal programming, it is the most plausible explanation for the extended period of low numbers following the population decline. Arctic ground squirrel males have an intense breeding season for two to three weeks in early spring, after which many of them die. The functioning of their stress axis changes markedly and is key in meeting their energy demands during this period. In contrast, red-backed vole males, though also short-lived, breed repeatedly only in the summer of their life, and their stress axis shows no change in function. However, their reproductive effort negatively affects their long-term survival. Territorial red squirrels experience marked interannual fluctuations in their major food source (white spruce seed), resulting in major fluctuations in their densities and consequently in the intensity of territorial competition. Changes in the densities of red squirrels also alter maternal stress hormone levels, inducing adaptive plasticity in offspring postnatal growth rates that prepares offspring for the environment they will encounter at independence. To survive winter, red squirrels need to defend their territories year-round, and the basis of this defense appears to be adrenal dehydroepiandrosterone, which has the benefits, but not the costs, of gonadal steroids. Arctic ground squirrels survive winter by hibernating in deeply frozen ground. Unlike all other hibernators, they have evolved a unique adaptation: high levels of adrenal androgens in summer to accumulate protein reserves that they then burn in winter. With a rapidly changing climate, the stress axis will play a key role in permitting northern animals to adapt, but the linkages between the changes in the abiotic and biotic components of the boreal forest and the phenotypic plasticity in the stress response of its inhabitants are not well understood for these or any other herbivore species.L’axe hypothalamo-hypophyso-surrénalien (l’axe du stress) joue un rôle central pour aider les mammifères à réussir dans l’environnement difficile de la forêt boréale. Ces 20 dernières années, nous nous sommes penchés sur une vaste gamme de sujets afin de comprendre comment fonctionne l’axe du stress chez quatre grandes espèces herbivores. Pour le lièvre d’Amérique, le défi central consiste à faire face à ses prédateurs, tandis que pour les autres espèces, ce défi consiste à se faire face mutuellement (surtout pendant la reproduction) de même qu’à faire face à leur environnement physique. Les lièvres subissent beaucoup de stress de la part de leurs prédateurs pendant la diminution de la population. La menace des prédateurs est la cause de changements majeurs sur l’axe du stress des lièvres, ce qui a pour effet de réduire leur reproduction. De plus, en raison de leur programmation maternelle, il s’agit de l’explication la plus plausible justifiant la période prolongée de leur faible nombre suivant la diminution de la population. Le spermophile arctique mâle a une période de reproduction intense pendant deux à trois semaines au début du printemps et après cela, un grand nombre d’entre eux meurent. Le fonctionnement de son axe de stress change de façon marquée, ce qui est essentiel à sa demande en énergie pendant cette période. Par contraste, le campagnol à dos roux mâle, même s’il ne vit également pas longtemps, se reproduit à répétition seulement pendant l’été de sa vie, et le fonctionnement de son axe de stress ne montre aucun changement. Cependant, ses efforts de reproduction ont des incidences négatives sur sa survie à long terme. Pour sa part, la principale source d’alimentation (les graines d’épinette blanche) de l’écureuil roux territorial connaît des fluctuations interannuelles marquées, ce qui se traduit par une fluctuation majeure en matière de densité de cette espèce animale et, par conséquent, en matière d’intensité de la concurrence pour le territoire. Les changements de densité d’écureuils roux exercent également une influence sur les taux d’hormone maternelle de stress, ce qui donne lieu à une plasticité adaptative des taux de croissance postnatale de la progéniture qui prépare la progéniture pour faire face à l’environnement dans lequel ils évolueront au stade de l’indépendance. Pour survivre à l’hiver, l’écureuil roux doit défendre son territoire à l’année et pour y parvenir, il se sert de la déhydroépiandrostérone surrénalienne, qui comporte les avantages des stéroïdes gonades, sans les coûts. Le spermophile arctique survit à l’hiver en hibernant dans le sol gelé en profondeur. Contrairement à tous les autres hibernateurs, il s’est développé une adaptation unique en son genre, soit des taux élevés d’androgènes surrénaliens en été qui lui permettent d’accumuler les réserves de protéines qu’il brûle ensuite pendant l’hiver. À la lumière du changement climatique rapide, l’axe de stress jouera un rôle-clé pour permettre aux animaux du Nord de s’adapter, mais les liens entre les changements des composantes abiotiques et biotiques de la forêt boréale et la plasticité phénotypique de la réaction de stress de ses habitants ne sont pas bien compris dans le cas de ces espèces herbivores ou de toute autre espèce herbivore

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

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

Best practices to maximize the use and reuse of quantitative and systems pharmacology models: recommendations from the United Kingdom quantitative and systems pharmacology network

The lack of standardization in the way that quantitative and systems pharmacology (QSP) models are developed, tested, and documented hinders their reproducibility, reusability, and expansion or reduction to alternative contexts. This in turn undermines the potential impact of QSP in academic, industrial, and regulatory frameworks. This article presents a minimum set of recommendations from the UK Quantitative and Systems Pharmacology Network (UK QSP Network) to guide QSP practitioners seeking to maximize their impact, and stakeholders considering the use of QSP models in their environment

Systems Biology Markup Language (SBML): Language Specification for Level 3 Version 2 Core Release 2

Computational models can help researchers to interpret data, understand biological functions, and make quantitative predictions. The Systems Biology Markup Language (SBML) is a file format for representing computational models in a declarative form that different software systems can exchange. SBML is oriented towards describing biological processes of the sort common in research on a number of topics, including metabolic pathways, cell signaling pathways, and many others. By supporting SBML as an input/output format, different tools can all operate on an identical representation of a model, removing opportunities for translation errors and assuring a common starting point for analyses and simulations. This document provides the specification for Release 2 of Version 2 of SBML Level 3 Core. The specification defines the data structures prescribed by SBML as well as their encoding in XML, the eXtensible Markup Language. Release 2 corrects some errors and clarifies some ambiguities discovered in Release 1. This specification also defines validation rules that determine the validity of an SBML document, and provides many examples of models in SBML form. Other materials and software are available from the SBML project website at http://sbml.org/

Herpes simplex virus encephalitis is a trigger of brain autoimmunity

In 5 prospectively diagnosed patients with relapsing post-herpes simplex encephalitis (HSE), N-methyl-D-aspartate receptor (NMDAR) antibodies were identified. Antibody synthesis started 1 to 4 weeks after HSE, preceding the neurological relapse. Three of 5 patients improved postimmunotherapy, 1 spontaneously, and 1 has started to improve. Two additional patients with NMDAR antibodies, 9 with unknown neuronal surface antibodies, and 1 with NMDAR and unknown antibodies, were identified during retrospective assessment of 34 HSE patients; the frequency of autoantibodies increased over time (serum, p=0.004; cerebrospinal fluid, p=0.04). The 3 retrospectively identified NMDAR antibody-positive patients also had evidence of relapsing post-HSE. Overall, these findings indicate that HSE triggers NMDAR antibodies and potentially other brain autoimmunity