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In evolutionary ecology, two classes of explanations are frequently invoked to explain "early life effects" on adult outcomes. Developmental constraints (DC) explanations contend that costs of early adversity arise from limitations adversity places on optimal development. Adaptive response (AR) hypotheses propose that later life outcomes will be worse when early and adult environments are poorly "matched." Here, we use recently proposed mathematical definitions for these hypotheses and a quadratic-regression based approach to test the long-term consequences of variation in developmental environments on fertility in wild baboons. We evaluate whether low rainfall and/or dominance rank during development predict three female fertility measures in adulthood, and whether any observed relationships are consistent with DC and/or AR. Neither rainfall during development nor the difference between rainfall in development and adulthood predicted any fertility measures. Females who were low-ranking during development had an elevated risk of losing infants later in life, and greater change in rank between development and adulthood predicted greater risk of infant loss. However, both effects were statistically marginal and consistent with alternative explanations, including adult environmental quality effects. Consequently, our data do not provide compelling support for either of these common explanations for the evolution of early life effects.

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The conditions animals experience during the early developmental stages of their lives can have critical ongoing effects on their future health, welfare, and proper development. In this paper we draw on evolutionary theory to improve our understanding of the processes of developmental programming, particularly Predictive Adaptive Responses (PAR) that serve to match offspring phenotype with predicted future environmental conditions. When these predictions fail, a mismatch occurs between offspring phenotype and the environment, which can have long-lasting health and welfare effects. Examples include metabolic diseases resulting from maternal nutrition and behavioral changes from maternal stress. An understanding of these processes and their evolutionary origins will help in identifying and providing appropriate developmental conditions to optimize offspring welfare. This serves as an example of the benefits of using evolutionary thinking within veterinary science and we suggest that in the same way that evolutionary medicine has helped our understanding of human health, the implementation of evolutionary veterinary science (EvoVetSci) could be a useful way forward for research in animal health and welfare.

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Meta-analysis is used to test a variant of a Developmental Origins of Adult Health and Disease (DOHaD)'s conjecture known as predictive adaptive response (PAR). According to it, individuals who are exposed to mismatches between adverse or constrained in utero conditions, on the one hand, and postnatal obesogenic environments, on the other, are at higher risk of developing adult chronic conditions, including obesity, type 2 diabetes (T2D), hypertension and cardiovascular disease. We argue that migrant populations from low and middle to high-income countries offer a unique opportunity to test the conjecture. A database was constructed from an exhaustive literature search of peer-reviewed papers published prior to May 2021 contained in PUBMED and SCOPUS using keywords related to migrants, DOHaD, and associated health outcomes. Random effects meta-regression models were estimated to assess the magnitude of effects associated with migrant groups on the prevalence rate of T2D and hypertension in adults and overweight/obesity in adults and children. Overall, we used 38 distinct studies and 78 estimates of diabetes, 59 estimates of hypertension, 102 estimates of overweight/obesity in adults, and 23 estimates of overweight/obesity in children. Our results show that adult migrants experience higher prevalence of T2D than populations at destination (PR 1.48; 95% CI 1.35-1.65) and origin (PR 1.80; 95% CI 1.40-2.34). Similarly, there is a significant excess of obesity prevalence in children migrants (PR 1.22; 95% CI 1.04-1.43) but not among adult migrants (PR 0.89; 95% CI 0.80-1.01). Although the total effect of migrant status on prevalence of hypertension is centered on zero, some migrant groups show increased risks. Finally, the size of estimated effects varies significantly by migrant groups according to place of destination. Despite limitations inherent to all meta-analyses and admitting that some of our findings may be accounted for alternative explanations, the present study shows empirical evidence consistent with selected PAR-like conjectures.

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Because residents and immigrants from group living species may experience fitness costs associated with permanent changes in group membership, we examined the hypothesis that females experiencing socially unstable or socially stable conditions during development compensate these costs by shaping the phenotype of their own offspring differently. Groups of adult females experiencing either socially stable or unstable conditions in the early social environment were assigned to either socially stable or unstable conditions in the social environment as adults. We quantified affiliative and agonistic interactions among the females during pregnancy and lactation of the focal female, maternal and allomaternal care, hypothalamic-anterior pituitary-adrenal axis (HPA) acute stress response, and early offspring growth. Social instability during breeding enhanced agonistic interactions among adult females, and offspring that experienced socially unstable conditions exhibited enhanced offspring care, regardless of adult environments. Neither social behavior, offspring care, acute stress physiology, nor early growth was influenced by early or adult social stability conditions. These findings imply that socially unstable conditions prime developing females to shape the phenotype of their offspring to prevent negative effects of socially unstable environments.

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External predictive adaptive response (PAR) models assume that developmental exposures to stress carry predictive information about the future state of the environment, and that development of a faster life history (LH) strategy in this context functions to match the individual to this expected harsh state. More recently internal PAR models have proposed that early somatic condition (i.e., physical health) critically regulates development of LH strategies to match expected future somatic condition. Here we test the integrative hypothesis that poor physical health mediates the relation between early adversity and faster LH strategies. Data were drawn from a longitudinal study (birth to age 16; N = 1,388) of mostly African American participants with prenatal substance exposure. Results demonstrated that both external environmental conditions early in life (prenatal substance exposure, socioeconomic adversity, caregiver distress/depression, and adverse family functioning) and internal somatic condition during preadolescence (birthweight/gestational age, physical illness) uniquely predicted the development of faster LH strategies in adolescence (as indicated by more risky sexual and aggressive behavior). Consistent with the integrative hypothesis, the effect of caregiver distress/depression on LH strategy was mostly mediated by worse physical health. Discussion highlights the implications of these findings for theory and research on stress, development, and health.

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In humans and other long-lived species, harsh conditions in early life often lead to profound differences in adult life expectancy. In response, natural selection is expected to accelerate the timing and pace of reproduction in individuals who experience some forms of early-life adversity. However, the adaptive benefits of reproductive acceleration following early adversity remain untested. Here, we test a recent version of this theory, the internal predictive adaptive response (iPAR) model, by assessing whether accelerating reproduction following early-life adversity leads to higher lifetime reproductive success. We do so by leveraging 48 y of continuous, individual-based data from wild female baboons in the Amboseli ecosystem in Kenya, including prospective, longitudinal data on multiple sources of nutritional and psychosocial adversity in early life; reproductive pace; and lifetime reproductive success. We find that while early-life adversity led to dramatically shorter lifespans, individuals who experienced early adversity did not accelerate their reproduction compared with those who did not experience early adversity. Further, while accelerated reproduction predicted increased lifetime reproductive success overall, these benefits were not specific to females who experienced early-life adversity. Instead, females only benefited from reproductive acceleration if they also led long lives. Our results call into question the theory that accelerated reproduction is an adaptive response to both nutritional and psychosocial sources of early-life adversity in baboons and other long-lived species.

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Across mammals, cues of developmental support, such as touching, licking or attentiveness, stimulate neural development, behavioural exploration and even overall body growth. Why should such fitness-related traits be so sensitive to developmental conditions? Here, we review what we term the 'developmental support hypothesis', a potential adaptive explanation of this plasticity. Neural development can be a costly process, in terms of time, energy and exposure. However, environmental variability may sometimes compromise parental care during this costly developmental period. We propose this environmental variation has led to the evolution of adaptive plasticity of neural and behavioural development in response to cues of developmental support, where neural development is stimulated in conditions that support associated costs. When parental care is compromised, offspring grow less and adopt a more resilient and stress-responsive strategy, improving their chances of survival in difficult conditions, similar to existing ideas on the adaptive value of early-life programming of stress. The developmental support hypothesis suggests new research directions, such as testing the adaptive value of reduced neural growth and metabolism in stressful conditions, and expanding the range of potential cues animals may attend to as indicators of developmental support. Considering evolutionary and ecologically appropriate cues of social support also has implications for promoting healthy neural development in humans. This article is part of the theme issue 'Life history and learning: how childhood, caregiving and old age shape cognition and culture in humans and other animals'.

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Early-life environmental conditions may generate cohort differences in individual fitness, subsequently affecting population growth rates. Three, nonmutually exclusive hypotheses predict the nature of these fitness differences: (1) silver spoon effects, where individuals born in good conditions perform better across the range of adult environments; (2) the "environmental saturation" hypothesis, where fitness differences only occur in intermediate adult environmental conditions; and (3) the "environmental matching" or "predictive adaptive response" (PAR) hypothesis, where fitness is highest when adult environmental conditions match those experienced in early life. We quantified the context-dependent effect of early-life environment on subsequent reproductive success, survival, and population growth rate (λ) of Svalbard reindeer, and explored how well it was explained by the three hypotheses. We found that good early-life conditions increased reproductive success compared to poor early-life conditions, but only when experiencing intermediate adult environmental conditions. This is the first example of what appears to be both "beneficial" and "detrimental environmental saturation" in a natural system. Despite weak early-life effects on survival, cohorts experiencing good early-life conditions contributed to higher population growth rates, when simulating realistic variation in adult environmental conditions. Our results show how the combination of a highly variable environment and biological constraints on fitness components can suppress silver spoon effects at both extremes of the adult environmental gradient.

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The early life environment can have profound, long-lasting effects on an individual's fitness. For example, early life quality might (a) positively associate with fitness (a silver spoon effect), (b) stimulate a predictive adaptive response (by adjusting the phenotype to the quality of the environment to maximize fitness) or (c) be obscured by subsequent plasticity. Potentially, the effects of the early life environment can persist beyond one generation, though the intergenerational plasticity on fitness traits of a subsequent generation is unclear. To study both intra- and intergenerational effects of the early life environment, we exposed a first generation of bank voles to two early life stimuli (variation in food and social environment) in a controlled environment. To assess possible intra-generational effects, the reproductive success of female individuals was investigated by placing them in large outdoor enclosures in two different, ecologically relevant environments (population densities). Resulting offspring were raised in the same population densities where they were conceived and their growth was recorded. When adult, half of the offspring were transferred to opposite population densities to evaluate their winter survival, a crucial fitness trait for bank voles. Our setup allowed us to assess: (a) do early life population density cues elicit an intra-generational adaptive response, that is a higher reproductive success when the density matches the early life cues and (b) can early life stimuli of one generation elicit an intergenerational adaptive response in their offspring, that is a higher growth and winter survival when the density matches the early life cues of their mother. Our results show that the early life environment directly affects the phenotype and reproductive success of the focal generation, but adaptive responses are only evident in the offspring. Growth of the offspring is maintained only when the environment matches their mother's early life environment. Furthermore, winter survival of offspring also tended to be higher in high population densities if their mothers experienced an competitive early life. These results show that the early life environment can contribute to maintain high fitness in challenging environments, but not necessarily in the generation experiencing the early life cues.

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Telomere length (TL) declines with age in most human tissues, and shorter TL appears to accelerate senescence. By contrast, men's sperm TL is positively correlated with age. Correspondingly, in humans, older paternal age at conception (PAC) predicts longer offspring TL. We have hypothesized that this PAC effect could persist across multiple generations, and thereby contribute to a transgenerational genetic plasticity that increases expenditures on somatic maintenance as the average age at reproduction is delayed within a lineage. Here, we examine TL data from 3282 humans together with PAC data across four generations. In this sample, the PAC effect is detectable in children and grandchildren. The PAC effect is transmitted through the matriline and patriline with similar strength and is characterized by a generational decay. PACs of more distant male ancestors were not significant predictors, although statistical power was limited in these analyses. Sensitivity analyses suggest that the PAC effect is linear, not moderated by offspring age, or maternal age, and is robust to controls for income, urbanicity and ancestry. These findings show that TL reflects the age at the reproduction of recent male matrilineal and patrilineal ancestors, with an effect that decays across generations.

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Numerous studies have shown that social adversity in early life can have long-lasting consequences for social behaviour in adulthood, consequences that may in turn be propagated to future generations. Given these intergenerational effects, it is puzzling why natural selection might favour such sensitivity to an individual's early social environment. To address this question, we model the evolution of social sensitivity in the development of helping behaviours, showing that natural selection indeed favours individuals whose tendency to help others is dependent on early-life social experience. In organisms with non-overlapping generations, we find that natural selection can favour positive social feedbacks, in which individuals who received more help in early life are also more likely to help others in adulthood, while individuals who received no early-life help develop low tendencies to help others later in life. This positive social sensitivity is favoured because of an intergenerational relatedness feedback: patches with many helpers tend to be more productive, leading to higher relatedness within the local group, which in turn favours higher levels of help in the next generation. In organisms with overlapping generations, this positive feedback is less likely to occur, and those who received more help may instead be less likely to help others (negative social feedback). We conclude that early-life social influences can lead to strong between-individual differences in helping behaviour, which can take different forms dependent on the life history in question. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

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Variation in early-life conditions can trigger developmental switches that lead to predictable individual differences in adult behaviour and physiology. Despite evidence for such early-life effects being widespread both in humans and throughout the animal kingdom, the evolutionary causes and consequences of this developmental plasticity remain unclear. The current issue aims to bring together studies of early-life effects from the fields of both evolutionary ecology and biomedicine to synthesise and advance current knowledge of how information is used during development, the mechanisms involved, and how early-life effects evolved. We hope this will stimulate further research into early-life effects, improving our understanding of why individuals differ and how this might influence their susceptibility to disease. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

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A discrepancy between the phenotype of an individual and that which would confer optimal responses in terms of fitness in an environment is termed 'mismatch'. Phenotype results from developmental plasticity, conditioned partly by evolutionary history of the species and partly by aspects of the developmental environment. We discuss two categories of such mismatch with reference primarily to nutrition and in the context of evolutionary medicine. The categories operate over very different timescales. A developmental mismatch occurs when the phenotype induced during development encounters a different environment post-development. This may be the result of wider environmental changes, such as nutritional transition between generations, or because maternal malnutrition or placental dysfunction give inaccurate information about the organism's likely future environment. An evolutionary mismatch occurs when there is an evolutionarily novel environment. Developmental plasticity may involve immediate adaptive responses (IARs) to preserve survival if an environmental challenge is severe, and/or predictive adaptive responses (PARs) if the challenge does not threaten survival, but there is a fitness advantage in developing a phenotype that will be better adapted later. PARs can have long-term adverse health consequences if there is a developmental mismatch. For contemporary humans, maternal constraint of fetal growth makes PARs likely even if there is no obvious IAR, and this, coupled with the pervasive nutritionally dense modern environment, can explain the widespread observations of developmental mismatch, particularly in populations undergoing nutritional transition. Both developmental and evolutionary mismatch have important public health consequences and implications for where policy interventions may be most effective. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

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Preterm birth is a significant public health problem worldwide, leading to substantial mortality in the newborn period, and a considerable burden of complications longer term, for affected infants and their carers. The fact that it is so common, and rates vary between different populations, raising the question of whether in some circumstances it might be an adaptive trait. In this review, we outline some of the evolutionary explanations put forward for preterm birth. We specifically address the hypothesis of the predictive adaptive response, setting it in the context of the Developmental Origins of Health and Disease, and explore the predictions that this hypothesis makes for the potential causes and consequences of preterm birth. We describe how preterm birth can be triggered by a range of adverse environmental factors, including nutrition, stress and relative socioeconomic status. Examining the literature for any associated longer-term phenotypic changes, we find no strong evidence for a marked temporal shift in the reproductive life-history trajectory, but more persuasive evidence for a re-programming of the cardiovascular and endocrine system, and a range of effects on neurodevelopment. Distinguishing between preterm birth as a predictive, rather than immediate adaptive response will depend on the demonstration of a positive effect of these alterations in developmental trajectories on reproductive fitness. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

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Environmental conditions during early development, from conception to sexual maturity, can have lasting consequences on fitness components. Although adult life span often accounts for much of the variation in fitness in long-lived animals, we know little about how early environment affects adult life span in the wild, and even less about whether these effects differ between the sexes. Using data collected over 45 years from wild bighorn sheep (Ovis canadensis), we investigated the effects of early environment on adult mortality in both sexes, distinguishing between natural and anthropogenic sources of mortality. We used the average body mass of yearlings (at about 15 months of age) as a yearly index of environmental quality. We first examined sex differences in natural mortality responses to early environment by censoring harvested males in the year they were shot. We then investigated sex differences in the effects of early environment on overall mortality (natural and hunting mortality combined). Finally, we used path analysis to separate the direct influence of early environment from indirect influences, mediated by age at first reproduction, adult mass and horn length. As early environmental conditions improved, natural adult mortality decreased in both sexes, although for males the effect was not statistically supported. Sex differences in the effects of early environment on adult mortality were detected only when natural and hunting mortality were pooled. Males that experienced favourable early environment had longer horns as adults and died earlier because of trophy hunting, which does not mimic natural mortality. Females that experienced favourable early environment started to reproduce earlier and early primiparity was associated with reduced mortality, suggesting a silver-spoon effect. Our results show that early conditions affect males and females differently because of trophy hunting. These findings highlight the importance of considering natural and anthropogenic environmental factors across different life stages to understand sex differences in mortality.

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Evidence has emerged that endocrine-disrupting chemicals (EDCs) can produce adverse effects, even at low doses that are assumed safe. However, systemic reviews and meta-analyses focusing on human studies, especially of EDCs with short half-lives, have demonstrated inconsistent results. Epidemiological studies have insuperable methodological limitations, including the unpredictable net effects of mixtures, non-monotonic dose-response relationships, the non-existence of unexposed groups, and the low reliability of exposure assessment. Thus, despite increases in EDC-linked diseases, traditional epidemiological studies based on individual measurements of EDCs in bio-specimens may fail to provide consistent results. The exposome has been suggested as a promising approach to address the uncertainties surrounding human studies, but it is never free from these methodological issues. Although exposure to EDCs during critical developmental periods is a major concern, continuous exposure to EDCs during non-critical periods is also harmful. Indeed, the evolutionary aspects of epigenetic programming triggered by EDCs during development should be considered because it is a key mechanism for developmental plasticity. Presently, living without EDCs is impossible due to their omnipresence. Importantly, there are lifestyles which can increase the excretion of EDCs or mitigate their harmful effects through the activation of mitohormesis or xenohormesis. Effectiveness of lifestyle interventions should be evaluated as practical ways against EDCs in the real world.

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Developmental plasticity, a phenomenon of importance in both evolutionary biology and human studies of the developmental origins of health and disease (DOHaD), enables organisms to respond to their environment based on previous experience without changes to the underlying nucleotide sequence. Although such phenotypic responses should theoretically improve an organism's fitness and performance in its future environment, this is not always the case. Herein, we first discuss epigenetics as an adaptive mechanism of developmental plasticity and use signaling theory to provide an evolutionary context for DOHaD phenomena within a generation. Next, we utilize signalling theory to identify determinants of adaptive developmental plasticity, detect sources of random variability - also known as process errors that affect maintenance of an epigenetic signal (DNA methylation) over time, and discuss implications of these errors for an organism's health and fitness. Finally, we apply life-course epidemiology conceptual models to inform study design and analytical strategies that are capable of parsing out the potential effects of process errors in the relationships among an organism's early environment, DNA methylation, and phenotype in a future environment. Ultimately, we hope to foster cross-talk and interdisciplinary collaboration between evolutionary biology and DOHaD epidemiology, which have historically remained separate despite a shared interest in developmental plasticity.

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Telomeres are repeating DNA found at the ends of chromosomes that, in the absence of restorative processes, shorten with cell replications and are implicated as a cause of senescence. It appears that sperm telomere length (TL) increases with age in humans, and as a result offspring of older fathers inherit longer telomeres. We review possible mechanisms underlying this paternal age at conception (PAC) effect on TL, including sperm telomere extension due to telomerase activity, age-dependent changes in the spermatogonial stem cell population (possibly driven by 'selfish' spermatogonia) and non-causal confounding. In contrast to the lengthening of TL with PAC, higher maternal age at conception appears to predict shorter offspring TL in humans. We review evidence for heterogeneity across species in the PAC effect on TL, which could relate to differences in statistical power, sperm production rates or testicular telomerase activity. Finally, we review the hypothesis that the PAC effect on TL may allow a gradual multi-generational adaptive calibration of maintenance effort, and reproductive lifespan, to local demographic conditions: descendants of males who reproduced at a later age are likely to find themselves in an environment where increased maintenance effort, allowing later reproduction, represents a fitness improving resource allocation.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.

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The mother is the major interface between the offspring and its prenatal environment. Prenatal toxins and stress-inducing physical agents are important factors programming the developmental trajectory of mammals that likely involve epigenetic modifications. However, prenatal stressors commonly-used in the laboratory (e.g. prenatal restraint stress and prenatal chronic variable stress) are typically administered at high intensities. These exposures typically lead to pathological phenotypes supporting the development origin of health and disease hypothesis. In this review, we compare the phenotypic outcomes of these commonly-used prenatal stressors to an ecologically-relevant, psychogenic stressor that has been present over evolutionary times, predator or predator cues presence. Prenatal stress by predator threat results in behavioral, physiological, endocrine, transcript abundance and epigenetic (DNA methylation) modifications. These phenotypic modifications are consistent with developmental forecasting according to the Predictive Adaptive Response hypothesis, yielding adaptive responses in environments where such predation stress is present. The evidence described in this review suggests that the type of prenatal stress agent and its intensity modifies the phenotype expressed, which can range from adaptive to pathological. Prenatal Bisphenol A exposure studies are presented as an example where graded intensities (concentrations) of prenatal toxin exposure can be compared directly. Finally, we emphasize the importance of studying both sexes in these studies, as sex differences appear to be a common feature of the response to prenatal stress.

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Evidence has emerged that endocrine-disrupting chemicals (EDCs) can produce adverse effects, even at low doses that are assumed safe. However, systemic reviews and meta-analyses focusing on human studies, especially of EDCs with short half-lives, have demonstrated inconsistent results. Epidemiological studies have insuperable methodological limitations, including the unpredictable net effects of mixtures, non-monotonic dose-response relationships, the non-existence of unexposed groups, and the low reliability of exposure assessment. Thus, despite increases in EDC-linked diseases, traditional epidemiological studies based on individual measurements of EDCs in bio-specimens may fail to provide consistent results. The exposome has been suggested as a promising approach to address the uncertainties surrounding human studies, but it is never free from these methodological issues. Although exposure to EDCs during critical developmental periods is a major concern, continuous exposure to EDCs during non-critical periods is also harmful. Indeed, the evolutionary aspects of epigenetic programming triggered by EDCs during development should be considered because it is a key mechanism for developmental plasticity. Presently, living without EDCs is impossible due to their omnipresence. Importantly, there are lifestyles which can increase the excretion of EDCs or mitigate their harmful effects through the activation of mitohormesis or xenohormesis. Effectiveness of lifestyle interventions should be evaluated as practical ways against EDCs in the real world.

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