Predictive Adaptive Response Research Articles

Long-term personality changes and predictive adaptive responses after depressive episodes

An external or internal “predictive adaptive response” (PAR) can be defined as an adaptive change in long-term behavior or development due to an environmental exposure that triggers it. A PAR can lead to differential development among initially similar individuals, and increase evolutionary fitness. Despite many theories and empirical observations of PAR-like changes in depressive tendencies, clear empirical findings on human personality changes following depressive symptoms are lacking, possibly because these changes take a long time to develop and most follow up studies have been short. Here we show that in sufficiently long (5- and 15-year) clinical and general-population follow ups, increases can be observed in the Temperament and Character Inventory's personality trait harm avoidance as a function of temporally accumulating major depressive episodes (132 depression patients from Vantaa Depression Study) and depressive symptoms (3105 participants from Young Finns general-population sample). Personality changes did not occur in the other six personality traits of the inventory, but did in a highly similar neuroticism trait from another inventory. Even when controlling for concurrent changes in depressive symptoms from the baseline to the endpoint, depressive symptoms that occurred during the follow-up period associated with harm-avoidance changes, rendering individuals more fearful and anticipating harm. This study provides consistent, specific, and plausible dose–response and temporal gradients between accumulated depressive episodes and personality change. Effect sizes were between small to moderate, though. Altogether, the findings support the feasibility of using existing systems of personality assessment (i.e., self-report questionnaires) to study PARs, despite the multiplicity of the systems.

Effect of prenatal exposure to LPS combined with pre- and post-natal high-fat diet on hippocampus in rat offspring

ObjectivePrenatal exposure to lipopolysaccharide (LPS) or high-fat diet (HFD) results in hippocampal impairment and cognitive deficits in offspring rats. What is not clear is how prenatal exposure to LPS combined with pre- and post-natal HFD would affect the hippocampus in offspring rats. Methods32 pregnant rats were randomly divided into four groups, including control group; LPS group (pregnant rats were injected with LPS 0.4mg/kg intraperitoneally on the 8th, 10th and 12th day of pregnancy); HFD group (maternal rats had HFD during pregnancy and the lactation period, and their pups also had HFD up to the third month of life); LPS+HFD group (rats were exposed to the identical experimental scheme with LPS group and HFD group). The serum IL-6 and TNF-alpha concentration was measured in three-month-old offspring rats in all groups. Hippocampal morphology and expressions of glial fibrillary acidic protein (GFAP), Tau and synaptophysin (SYP) in offspring rats were measured. ResultsSerum IL-6 and TNF-alpha concentration in the HFD group increased significantly compared with the control group, LPS group and LPS+HFD group. Compared with the control group and the LPS+HFD group, cells in the LPS and HFD groups were smaller and arranged in disorder, and cell membrane was not complete, nucleoli and nuclear heterochromatin stained darkly with hematoxylin. GFAP and Tau expression in the hippocampus of the LPS and HFD groups increased significantly compared with the control group and LPS+HFD group. SYP expression in the LPS and HFD groups decreased significantly compared with the control group and HFD group, increased in the LPS+HFD group. ConclusionPrenatal exposure to LPS combined with pre- and post-natal HFD result in a protective effect on the hippocampus in offspring rats, and it might be a benefit from the predictive adaptive response to prenatal inflammation.

Inborn stress reactivity shapes adult behavioral consequences of early-life maternal separation stress

Early-life experience strongly impacts neurodevelopment and stress susceptibility in adulthood. Maternal separation (MS), an established model of early-life adversity, has been shown to negatively impact behavioral and endocrine responses to stress in adulthood. However, the impact of MS in rats with heightened inborn stress susceptibility has not been fully explored. To address this issue we conducted MS in Wistar-Kyoto (WKY) rats, an animal model of comorbid depression and anxiety, and Wistar rats, which share a similar genetic background with WKYs. WKY and Wistar pups experienced either 180-min daily MS or 15-min separation (neonatal handling) during the first two postnatal weeks, and were tested for depressive- and anxiety- like behaviors in adulthood. Exposure to early-life MS in WKY rats decreased anxiety- and depressive- like behaviors, leading to increased exploration on the open field test (OFT), enhanced social interaction, and diminished immobility on the forced swim test. MS had an opposite effect in Wistar offspring, leading to enhanced anxiety-like behaviors, such as reduced OFT exploration and decreased social interaction. These findings are consistent with the match/mismatch theory of disease and the predictive adaptive response, which suggests that early life stress exposure can confer adaptive value in later life within certain individuals. Our data supports this theory, showing that early-life MS has positive and perhaps adaptive effects within stress-vulnerable WKY offspring. Future studies will be required to elucidate the neurobiological underpinnings of contrasting behavioral effects of MS on WKY vs. Wistar offspring.

Fetal ultrasound measurements and associations with postnatal outcomes in infancy and childhood: a systematic review of an emerging literature

BackgroundSeveral hypotheses predict that faltering fetal growth is an antecedent for common non-communicable diseases. This is the first systematic review of an emerging literature linking antenatal fetal measurements to postnatal...

Plasticity and constraint in response to early-life stressors among late/final Jomon period foragers from Japan: evidence for life history trade-offs from incremental microstructures of enamel.

This study evaluates two hypotheses that address how Late/Final Jomon period people responded to early-life stress using linear enamel hypoplasia (LEH) and incremental microstructures of enamel. The first hypothesis predicts that Jomon people who experienced early-life stressors had greater physiological competence in responding to future stress events (predictive adaptive response). The second hypothesis predicts that Jomon people traded-off in future growth and maintenance when early investment in growth and survival was required (plasticity/constraint). High resolution tooth impressions were collected from intact, anterior teeth and studied under an engineer's measuring microscope. LEH were identified based on accentuated perikymata and depressions in the enamel surface profile. Age of formation for each LEH was estimated by summing counts of perikymata and constants associated with crown initiation and cuspal enamel formation times. The relationship between age-at-first-defect formation, number of LEH, periodicity between LEH, and mortality was evaluated using multiple regression and hazards analysis. A significant, positive relationship was found between age-at-death relative to age-at-first-defect formation and a significant, negative relationship was found between number of LEH relative to age-at-first-defect formation. Individuals with earlier forming defects were at a significantly greater risk of forming defects at later stages of development and dying at younger ages. These results suggest that Late/Final Jomon period foragers responded to early-life stressors in a manner consistent with the plasticity/constraint hypothesis of human life history. Late/Final Jomon period individuals were able to survive early-life stressors, but this investment weakened responses to future stress events and exacerbated mortality schedules.

Fitness consequences of environmental conditions at different life stages in a long-lived vertebrate.

The predictive adaptive response (PAR) hypothesis proposes that animals adjust their physiology and developmental trajectory during early life in anticipation of their future environments. Accordingly, when environmental conditions in early life match environmental conditions during adulthood, individual fitness should be greater. Here, we test this hypothesis in a long-lived mammal, the roe deer, using data from two contrasting populations, intensively monitored for more than 35 years. In the highly productive site, the fitness of female roe deer increased with the quality of environment during adulthood and, contrary to predictions of PAR, individuals born in good conditions always outperformed those born under poor conditions. In the resource-limited site, the fitness of female roe deer born in poor years was better than those born in good conditions in poor years when the animals were adult, but not in good years. Although consistent with predictions of PAR, we showed that this pattern is likely to be a consequence of increased viability selection during the juvenile stage for animals born in poor years. While PARs are often advanced in evolutionary medicine, our findings suggest that detailed biological processes should be investigated before drawing conclusions about the existence of this phenomenon.

The biology of developmental plasticity and the Predictive Adaptive Response hypothesis.

Many forms of developmental plasticity have been observed and these are usually beneficial to the organism. The Predictive Adaptive Response (PAR) hypothesis refers to a form of developmental plasticity in which cues received in early life influence the development of a phenotype that is normally adapted to the environmental conditions of later life. When the predicted and actual environments differ, the mismatch between the individual's phenotype and the conditions in which it finds itself can have adverse consequences for Darwinian fitness and, later, for health. Numerous examples exist of the long-term effects of cues indicating a threatening environment affecting the subsequent phenotype of the individual organism. Other examples consist of the long-term effects of variations in environment within a normal range, particularly in the individual's nutritional environment. In mammals the cues to developing offspring are often provided by the mother's plane of nutrition, her body composition or stress levels. This hypothetical effect in humans is thought to be important by some scientists and controversial by others. In resolving the conflict, distinctions should be drawn between PARs induced by normative variations in the developmental environment and the ill effects on development of extremes in environment such as a very poor or very rich nutritional environment. Tests to distinguish between different developmental processes impacting on adult characteristics are proposed. Many of the mechanisms underlying developmental plasticity involve molecular epigenetic processes, and their elucidation in the context of PARs and more widely has implications for the revision of classical evolutionary theory.

Evolution evolves: physiology returns to centre stage

Denis Noble, Eva Jablonka, Michael J. Joyner, Gerd B. Muller and Stig W. Omholt University of Oxford, Department of Physiology, Anatomy and Genetics, Oxford, UK Tel Aviv University, Cohn Institute for the History andPhilosophyof Science and Ideas, Ramat Aviv, Israel Mayo Clinic, Rochester, MN, USA University of Vienna, Department of Theoretical Biology, Vienna, Austria Norwegian University of Science and Technology, Faculty of Medicine, Trondheim, Norway

Early stress and human behavioral development: emerging evolutionary perspectives.

Stress experienced early in life exerts a powerful, lasting influence on development. Converging empirical findings show that stressful experiences become deeply embedded in the child's neurobiology, with an astonishing range of long-term effects on cognition, emotion, and behavior. In contrast with the prevailing view that such effects are the maladaptive outcomes of 'toxic' stress, adaptive models regard them as manifestations of evolved developmental plasticity. In this paper, I offer a brief introduction to adaptive models of early stress and human behavioral development, with emphasis on recent theoretical contributions and emerging concepts in the field. I begin by contrasting dysregulation models of early stress with their adaptive counterparts; I then introduce life history theory as a unifying framework, and review recent work on predictive adaptive responses (PARs) in human life history development. In particular, I discuss the distinction between forecasting the future state of the environment (external prediction) and forecasting the future state of the organism (internal prediction). Next, I present the adaptive calibration model, an integrative model of individual differences in stress responsivity based on life history concepts. I conclude by examining how maternal-fetal conflict may shape the physiology of prenatal stress and its adaptive and maladaptive effects on postnatal development. In total, I aim to show how theoretical work from evolutionary biology is reshaping the way we think about the role of stress in human development, and provide researchers with an up-to-date conceptual map of this fascinating and rapidly evolving field.

The evolution of predictive adaptive responses in humans: response

The evolution of predictive adaptive responses in humans: response

Life history plasticity in humans: the predictive value of early cues depends on the temporal structure of the environment

Nettle et al. [[1][1]] explored the conditions under which it could be adaptive for humans to calibrate the development of life history traits (for example, reproductive timing) on the level of adversity experienced in early life. They concluded that external predictive adaptive responses (PARs)—

Embryonic thermosensitive TRPA1 determines transgenerational diapause phenotype of the silkworm,Bombyx mori

In the bivoltine strain of the silkworm, Bombyx mori, embryonic diapause is induced transgenerationally as a maternal effect. Progeny diapause is determined by the environmental temperature during embryonic development of the mother; however, its molecular mechanisms are largely unknown. Here, we show that the Bombyx TRPA1 ortholog (BmTrpA1) acts as a thermosensitive transient receptor potential (TRP) channel that is activated at temperatures above ∼ 21 °C and affects the induction of diapause in progeny. In addition, we show that embryonic RNAi of BmTrpA1 affects diapause hormone release during pupal-adult development. This study identifying a thermosensitive TRP channel that acts as a molecular switch for a relatively long-term predictive adaptive response by inducing an alternative phenotype to seasonal polyphenism is unique.

Prenatal Exposure to Lipopolysaccharide Combined with Pre- and Postnatal High-Fat Diet Result in Lowered Blood Pressure and Insulin Resistance in Offspring Rats

BackgroundAdult metabolic syndrome may in part have origins in fetal or early life. This study was designed to explore the effect of prenatal exposure to lipopolysaccharide and high-fat diet on metabolic syndrome in offspring rats.Methods32 pregnant rats were randomly divided into four groups, including Control group; LPS group (pregnant rats were injected with LPS 0.4 mg/kg intraperitoneally on the 8th, 10th and 12th day of pregnancy); High-fat group (maternal rats had high-fat diet during pregnancy and lactation period, and their pups also had high-fat diet up to the third month of life); LPS + High-fat group (rats were exposed to the identical experimental scheme with LPS group and High-fat group).ResultsBlood pressure elevated in LPS group and High-fat group, reduced in LPS+High-fat group, accompanied by the increase of serum leptin level in LPS and High-fat group and increase of serum IL-6, TNF-a in High-fat group; both serum insulin and cholesterol increased in High-fat and LPS+High-fat group, as well as insulin in LPS group. HOMA-IR value increased in LPS, High-fat and LPS+High-fat group, and QUICKI decreased in these groups; H-E staining showed morphologically pathological changes in thoracic aorta and liver tissue in the three groups. Increased serum alanine and aspartate aminotransferase suggest impaired liver function in LPS+High-fat group.Conclusion/SignificancePrenatal exposure to lipopolysaccharide combined with pre- and postnatal high-fat diet result in lowered blood pressure, insulin resistance and impaired liver function in three-month old offspring rats. The lowered blood pressure might benefit from the predictive adaptive response to prenatal inflammation.

The evolution of predictive adaptive responses in human life history.

Many studies in humans have shown that adverse experience in early life is associated with accelerated reproductive timing, and there is comparative evidence for similar effects in other animals. There are two different classes of adaptive explanation for associations between early-life adversity and accelerated reproduction, both based on the idea of predictive adaptive responses (PARs). According to external PAR hypotheses, early-life adversity provides a 'weather forecast' of the environmental conditions into which the individual will mature, and it is adaptive for the individual to develop an appropriate phenotype for this anticipated environment. In internal PAR hypotheses, early-life adversity has a lasting negative impact on the individual's somatic state, such that her health is likely to fail more rapidly as she gets older, and there is an advantage to adjusting her reproductive schedule accordingly. We use a model of fluctuating environments to derive evolveability conditions for acceleration of reproductive timing in response to early-life adversity in a long-lived organism. For acceleration to evolve via the external PAR process, early-life cues must have a high degree of validity and the level of annual autocorrelation in the individual's environment must be almost perfect. For acceleration to evolve via the internal PAR process requires that early-life experience must determine a significant fraction of the variance in survival prospects in adulthood. The two processes are not mutually exclusive, and mechanisms for calibrating reproductive timing on the basis of early experience could evolve through a combination of the predictive value of early-life adversity for the later environment and its negative impact on somatic state.

Influence of early-life nutrition on mortality and reproductive success during a subsequent famine in a preindustrial population

Individuals with insufficient nutrition during development often experience poorer later-life health and evolutionary fitness. The Predictive Adaptive Response (PAR) hypothesis proposes that poor early-life nutrition induces physiological changes that maximize fitness in similar environments in adulthood and that metabolic diseases result when individuals experiencing poor nutrition during development subsequently encounter good nutrition in adulthood. However, although cohort studies have shown that famine exposure in utero reduces health in favorable later-life conditions, no study on humans has demonstrated the predicted fitness benefit under low later-life nutrition, leaving the evolutionary origins of such plasticity unexplored. Taking advantage of a well-documented famine and unique datasets of individual life histories and crop yields from two preindustrial Finnish populations, we provide a test of key predictions of the PAR hypothesis. Known individuals from fifty cohorts were followed from birth until the famine, where we analyzed their survival and reproductive success in relation to the crop yields around birth. We were also able to test whether the long-term effects of early-life nutrition differed between individuals of varying socioeconomic status. We found that, contrary to predictions of the PAR hypothesis, individuals experiencing low early-life crop yields showed lower survival and fertility during the famine than individuals experiencing high early-life crop yields. These effects were more pronounced among young individuals and those of low socioeconomic status. Our results do not support the hypothesis that PARs should have been favored by natural selection and suggest that alternative models may need to be invoked to explain the epidemiology of metabolic diseases.

Organizational Changes to Thyroid Regulation in Alligator mississippiensis: Evidence for Predictive Adaptive Responses

During embryonic development, organisms are sensitive to changes in thyroid hormone signaling which can reset the hypothalamic-pituitary-thyroid axis. It has been hypothesized that this developmental programming is a ‘predictive adaptive response’, a physiological adjustment in accordance with the embryonic environment that will best aid an individual's survival in a similar postnatal environment. When the embryonic environment is a poor predictor of the external environment, the developmental changes are no longer adaptive and can result in disease states. We predicted that endocrine disrupting chemicals (EDCs) and environmentally-based iodide imbalance could lead to developmental changes to the thyroid axis. To explore whether iodide or EDCs could alter developmental programming, we collected American alligator eggs from an estuarine environment with high iodide availability and elevated thyroid-specific EDCs, a freshwater environment contaminated with elevated agriculturally derived EDCs, and a reference freshwater environment. We then incubated them under identical conditions. We examined plasma thyroxine and triiodothyronine concentrations, thyroid gland histology, plasma inorganic iodide, and somatic growth at one week (before external nutrition) and ten months after hatching (on identical diets). Neonates from the estuarine environment were thyrotoxic, expressing follicular cell hyperplasia (p = 0.01) and elevated plasma triiodothyronine concentrations (p = 0.0006) closely tied to plasma iodide concentrations (p = 0.003). Neonates from the freshwater contaminated site were hypothyroid, expressing thyroid follicular cell hyperplasia (p = 0.01) and depressed plasma thyroxine concentrations (p = 0.008). Following a ten month growth period under identical conditions, thyroid histology (hyperplasia p = 0.04; colloid depletion p = 0.01) and somatic growth (body mass p<0.0001; length p = 0.02) remained altered among the contaminated sites. This work supports the hypothesis that embryonic EDC exposure or iodide imbalance could induce adult metabolic disease states, thereby stressing the need to consider the multiple environmental variables present during development.

The Predictive Adaptive Response: Modeling the Life-History Evolution of the ButterflyBicyclus anynanain Seasonal Environments

A predictive adaptive response (PAR) is a type of developmental plasticity where the response to an environmental cue is not immediately advantageous but instead is later in life. The PAR is a way for organisms to maximize fitness in varying environments. Insects living in seasonal environments are valuable model systems for testing the existence and form of PAR. Previous manipulations of the larval and the adult environments of the butterfly Bicyclus anynana have shown that individuals that were food restricted during the larval stage coped better with forced flight during the adult stage compared to those with optimal conditions in the larval stage. Here, we describe a state-dependent energy allocation model, which we use to test whether such a response to food restriction could be adaptive in nature where this butterfly exhibits seasonal cycles. The results from the model confirm the responses obtained in our previous experimental work and show how such an outcome was facilitated by resource allocation patterns to the thorax during the pupal stage. We conclude that for B. anynana, early-stage cues can direct development toward a better adapted phenotype later in life and, therefore, that a PAR has evolved in this species.

Perinatal programming of obesity: an introduction to the topic

Perinatal programming of obesity: an introduction to the topic

Testing the evolutionary basis of the predictive adaptive response hypothesis in a preindustrial human population

The thrifty phenotype hypothesis proposes that late-life metabolic diseases result from mismatch between early-life and adulthood nutrition. More recently, the predictive adaptive response (PAR) hypothesis has suggested that poor early-life environmental conditions induce metabolic changes that maximize health and fitness in similarly poor adult conditions, but reduce fitness if conditions later improve. Therefore, later-life survival and reproduction should be maximized where environmental conditions during development and adulthood match, but few studies in humans have addressed the consequences of poor early conditions on fitness traits in varying later conditions. We tested key evolutionary predictions of the PAR hypothesis using detailed longitudinal data with several environmental parameters from a natural fertility preindustrial human population, to investigate how combinations of early- and late-life environmental conditions affected annual probabilities of survival and reproduction. We found no suggestion that fitness was maximised when developmental and later-life conditions matched, but rather poor environmental conditions during development or later life and their combinations were associated with lower survival. Our results are more consistent with predictions of 'silver spoon' models, whereby adverse early-life conditions are detrimental to later health and fitness across all environments. Future evolutionary research on understanding metabolic disease epidemiology should focus on determining whether adaptive prediction maximizes infant survival where conditions match during development and immediately after birth, rather than drawing attention to the unlikely long-term fitness benefits of putative metabolic changes associated with poor early nutrition.

Lessons from the life history of natural fertility societies on child growth and maturation

During the evolution of hominids, childhood and adolescence have been added as new life-history phases. The transition from infancy to childhood (ICT) confers a predictive adaptive response to energetic cues that strongly influence adult height, whereas the transition from juvenility to adolescence establishes longevity and the age of fertility. Evolutionary short-term adaptations to energy crises apparently use epigenetic mechanisms that defer the ICT, culminating in short stature. The study of hunter-gatherers gives us an indication of pre-demographic transition populations and their life style that prevailed for 99% of homo's evolution. The secular trend for receding age of pubertal development has been an adaptive response to positive environmental cues in terms of energy balance. In natural fertility preindustrial societies with limited access to modern contraception and health care, and whose economies are primarily subsistence-based, most resources are invested as somatic capital in human body size and fertility. Here we review results from databases for natural fertility societies, with the information on life history, population density, height and body mass, indices of adolescence and fertility. By using them it was possible to verify the ICT model as well as to explore pubertal parameters that are related to evolutionary fitness. They confirmed that body size was adaptively smaller in hostile environments, and was tightly associated with reproductive fitness.