Cumulative adversity and survival in the wild.

Protecting populations contending with co-occurring stressors requires a better understanding of how multiple early-life stressors affect the fitness of natural systems. However, the complexity of such research has limited its advancement and prevented us from answering new questions. In human studies, cumulative risk models predict adult health risk based on early adversity exposure. We apply a similar framework in wild yellow-bellied marmots (Marmota flaviventer). We tested cumulative adversity indices (CAIs) across different adversity types and time windows. All CAIs were associated with decreased pup survival and were well supported. Moderate and acute, but not standardized CAIs were associated with decreased lifespan, supporting the cumulative stress hypothesis and the endurance of early adversity. Multivariate models showed that differences in lifespan were driven by weaning date, precipitation, and maternal loss, but they performed poorly compared with CAI models. We highlight the development, utility, and insights of CAI approaches for ecology and conservation.

Vestiges of famine: Long-term mortality impacts of early-life exposure to the 1840s famine in Estonia.

The paper investigates whether exposure to a famine in the Russian Tsarist Province of Livland in 1844-1846 in early life negatively affected survival at later ages, using individual data from two rural parishes. We follow 18 birth cohorts born between 1834-1852 until age 75 and differentiate between timing and length of exposures. We find that relative to individuals born in pre- or post- crisis years, there were no significant differences in survival from age 21-75. Cohorts with longer exposure to famine conditions had increased mortality only in short term, up to age 20. Males were more vulnerable in younger ages than females. The negative effect of adverse early life exposure on survival in later life was constrained to lower social group - the landless, but for the better-off groups the effect was constrained to younger ages. The paper highlights the importance of accounting for sex and socio-economic differences in studies exploring the effects of early life conditions on later-life survival.

Early social complexity influences social behaviour but not social trajectories in a cooperatively breeding cichlid fish.

Social competence-defined as the ability to optimize social behaviour according to available social information-can be influenced by the social environment experienced in early life. In cooperatively breeding vertebrates, the current group size influences behavioural phenotypes, but it is not known whether the group size experienced in early life influences behavioural phenotypes generally or social competence specifically. We tested whether being reared in large versus small groups for the first two months of life affects social behaviours, and associated life-history traits, in the cooperatively breeding cichlid Neolamprologus pulcher between the ages of four and twelve months. As we predicted, fish raised in larger and more complex groups showed higher social competence later in life. This was shown in several ways: they exhibited more, and earlier, submissive behaviour in response to aggression from a dominant conspecific, and-in comparison to fish raised in small groups-they exhibited more flexibility in the expression of submissive behaviour. By contrast, there was no evidence that early social complexity, as captured by the group size, affects aggression or exploration behaviour nor did it influence the propensity to disperse or show helping behaviour. Our results emphasize the importance of early-life social complexity for the development of social competence.

Mother of all bonds: Influences on spatial association across the lifespan in capuchins.

In humans, being more socially integrated is associated with better physical and mental health and/or with lower mortality. This link between sociality and health may have ancient roots: sociality also predicts survival or reproduction in other mammals, such as rats, dolphins, and non-human primates. A key question, therefore, is which factors influence the degree of sociality over the life course. Longitudinal data can provide valuable insight into how environmental variability drives individual differences in sociality and associated outcomes. The first year of life-when long-lived mammals are the most reliant on others for nourishment and protection-is likely to play an important role in how individuals learn to integrate into groups. Using behavioral, demographic, and pedigree information on 376 wild capuchin monkeys (Cebus imitator) across 20 years, we address how changes in group composition influence spatial association. We further try to determine the extent to which early maternal social environments have downstream effects on sociality across the juvenile and (sub)adult stages. We find a positive effect of early maternal spatial association, where female infants whose mothers spent more time around others also later spent more time around others as juveniles and subadults. Our results also highlight the importance of kin availability and other aspects of group composition (e.g., group size) in dynamically influencing spatial association across developmental stages. We bring attention to the importance of-and difficulty in-determining the social versus genetic influences that parents have on offspring phenotypes. RESEARCH HIGHLIGHTS: Having more maternal kin (mother and siblings) is associated with spending more time near others across developmental stages in both male and female capuchins. Having more offspring as a subadult or adult female is additionally associated with spending more time near others. A mother's average sociality (time near others) is predictive of how social her daughters (but not sons) become as juveniles and subadults (a between-mother effect). Additional variation within sibling sets in this same maternal phenotype is not predictive of how social they become later relative to each other (no within-mother effect).

Natal legacies cause social and spatial marginalization during dispersal.

Early-life experiences can drive subsequent variation in social behaviours, but how differences among individuals emerge remains unknown. We combined experimental manipulations with GPS-tracking to investigate the pathways through which developmental conditions affect social network position during the early dispersal of wild red kites (Milvus milvus). Across 211 juveniles from 140 broods, last-hatched chicks-the least competitive-had the fewest number of peer encounters after fledging. However, when food supplemented, they had more encounters than all others. Using 4425 bird-days of GPS data, we revealed that this was driven by differential responses to competition, with less competitive individuals naturally spreading out into marginal areas, and clustering in central foraging areas when food supplemented. Our results suggest that early-life adversities can cause significant natal legacies on individual behaviour beyond independence, with potentially far-reaching consequences on the social and spatial structure of animal populations.

Conceptual and analytical approaches for modelling the developmental origins of inequality.

In many species, individuals that experience harsh conditions during development have poor health and fitness outcomes in adulthood, compared with peers that do not. These early-life contributions to inequality are often attributed to two classes of evolutionary hypotheses: Developmental Constraints (DC) models, which focus on the deleterious effects of low-quality early-life environments, and Predictive Adaptive Response (PAR) hypotheses, which emphasize the costs individuals incur when they make incorrect predictions about conditions in adulthood. Testing these hypotheses empirically is difficult for conceptual and analytical reasons. Here, we help resolve some of these difficulties by providing mathematical definitions for DC, PAR (particularly focusing on 'external' PAR) and related concepts. We propose a novel, quadratic regression-based statistical test derived from these definitions. Our simulations show that this approach markedly improves the ability to discriminate between DC and PAR hypotheses relative to the status quo approach, which uses interaction effects. Simulated data indicate that the interaction effects approach often conflates PAR with DC, while the quadratic regression approach yields high sensitivity and specificity for detecting PAR. Our results highlight the value of linking verbal and visual models to a formal mathematical treatment for understanding the developmental origins of inequitable adult outcomes. This article is part of the theme issue 'Evolutionary ecology of inequality'.

The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population.

Research in medicine and evolutionary biology suggests that the sequencing of parental investment has a crucial impact on offspring life history and health. Here, we take advantage of the synchronous birth system of wild banded mongooses to test experimentally the lifetime consequences to offspring of receiving extra investment prenatally versus postnatally. We provided extra food to half of the breeding females in each group during pregnancy, leaving the other half as matched controls. This manipulation resulted in two categories of experimental offspring in synchronously born litters: (i) 'prenatal boost' offspring whose mothers had been fed during pregnancy, and (ii) 'postnatal boost' offspring whose mothers were not fed during pregnancy but who received extra alloparental care in the postnatal period. Prenatal boost offspring lived substantially longer as adults, but postnatal boost offspring had higher lifetime reproductive success (LRS) and higher glucocorticoid levels across the lifespan. Both types of experimental offspring had higher LRS than offspring from unmanipulated litters. We found no difference between the two experimental categories of offspring in adult weight, age at first reproduction, oxidative stress or telomere lengths. These findings are rare experimental evidence that prenatal and postnatal investments have distinct effects in moulding individual life history and fitness in wild mammals. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Cumulative early-life adversity does not predict reduced adult longevity in wild gorillas.

Extensive research across fields has repeatedly confirmed that early-life adversity (ELA) is a major selective force for many taxa, in part via its ties to adult health and longevity.1,2,3 Negative effects of ELA on adult outcomes have been documented in a wide range of species, from fish to birds to humans.4 We used 55 years of long-term data collected on 253 wild mountain gorillas to examine the effects of six putative sources of ELA on survival, both individually and cumulatively. Although cumulative ELA was associated with high mortality in early life, we found no evidence that it had detrimental consequences for survival later in life. Experiencing three or more forms of ELA was associated with greater longevity, with a 70% reduction in the risk of death across adulthood, driven specifically by greater longevity in males. Although this higher survival in later life is likely a consequence of sex-specific viability selection5 during early life due to the immediate mortality consequences of adverse experiences, patterns in our data also suggest that gorillas have significant resilience to ELA. Our findings demonstrate that the detrimental consequences of ELA on later life survival are not universal, and indeed largely absent in one of humans' closest living relatives. This raises important questions about the biological roots of sensitivity to early experiences and the protective mechanisms that contribute to resiliency in gorillas, which could be critical for understanding how best to encourage similar resiliency to early-life shocks in humans.

Effects of early-life voluntary exercise and fructose on adult activity levels, body composition, aerobic capacity, and organ masses in mice bred for high voluntary wheel-running behavior.

Fructose (C6H12O6) is acutely obesogenic and is a risk factor for hypertension, cardiovascular disease, and nonalcoholic fatty liver disease. However, the possible long-lasting effects of early-life fructose consumption have not been studied. We tested for effects of early-life fructose and/or wheel access (voluntary exercise) in a line of selectively bred High Runner (HR) mice and a non-selected Control (C) line. Exposures began at weaning and continued for 3 weeks to sexual maturity, followed by a 23-week "washout" period (equivalent to ∼17 human years). Fructose increased total caloric intake, body mass, and body fat during juvenile exposure, but had no effect on juvenile wheel running and no important lasting effects on adult physical activity or body weight/composition. Interestingly, adult maximal aerobic capacity (VO2max) was reduced in mice that had early-life fructose and wheel access. Consistent with previous studies, early-life exercise promoted adult wheel running. In a 3-way interaction, C mice that had early-life fructose and no wheel access gained body mass in response to 2 weeks of adult wheel access, while all other groups lost mass. Overall, we found some long-lasting positive effects of early-life exercise, but minimal effects of early-life fructose, regardless of the mouse line.

Losing a parent in early-life impairs flock size discrimination and lowers oxytocin receptor abundance in a medial amygdala homologue of adult zebra finches.

Experiencing inadequate parental care during early-life diminishes adult social competencies. For example, low parental care impairs adult socio-cognitive abilities (e.g., recognizing familiar conspecifics) and affiliation (e.g., close social proximity); outcomes attributed to diminished medial amygdala nonapeptide functioning in rodents. Whether parental care has effects beyond familiarity, and if siblings have similar effects to parents, is unclear. Here, zebra finches were used to explore if parent and/or sibling number shape adult recognition and preference of small versus large flocks and nonapeptide (oxytocin, vasotocin) receptor expression in an avian homologue of the mammalian medial amygdala. Chicks were raised by single mothers or fathers in small broods or paired parents in small or large broods matched to single parents for chicks per nest or per parent, respectively. Pair-raised birds had preferred flock sizes as adults, but birds raised by single parents had equal preference for either size. Oxytocin receptor expression was lower in birds raised by single parents versus paired parents, but vasotocin receptor levels were unaffected. Such results highlight parents as formative antecedents of their offspring's social competencies related to group size preference and their nonapeptide mechanisms, outcomes that influence an animal's ability to live in social groups.

Effects of early-life exposure to Western diet and voluntary exercise on adult activity levels, exercise physiology, and associated traits in selectively bred High Runner mice.

Exercise behavior is under partial genetic control, but it is also affected by numerous environmental factors, potentially including early-life experiences whose effects persist into adulthood. We studied genetic and early-life environmental effects on wheel-running behavior in a mouse model that includes four replicate high runner (HR) lines selectively bred for increased voluntary wheel running as young adults and four non-selected control (C) lines. In a full factorial design, mice from each line were granted wheel access or not and administered either standard or Western diet (WD) from weaning (3 weeks old) to 6 weeks of age (sexual maturity). In addition to acute effects, after a washout period of 8 weeks (∼6 human years) in which all mice had standard diet and no wheel access, we found both beneficial and detrimental effects of these early-life exposures. During the first week of treatments, WD increased distance run by 29% in C mice and 48% in HR mice (significant Diet × Linetype interaction), but diet effects disappeared by the third week. Across the three weeks of juvenile treatment, WD significantly increased fat mass (with lean mass as a covariate). Tested as adults, early-life exercise increased wheel running of C mice but not HR mice in the first week. Early-life exercise also reduced adult anxiety-like behavior and increased adult fasted blood glucose levels, triceps surae mass, subdermal fat pad mass, and brain mass, but decreased heart ventricle mass. Using fat mass as a covariate, early-life exercise treatment increased adult leptin concentration. In contrast, early-life WD increased adult wheel running of HR mice but not C mice. Early-life WD also increased adult lean mass and adult preference for Western diet in all groups. Surprisingly, early-life treatment had no significant effect on adult body fat or maximal aerobic capacity (VO2max). No previous study has tested for combined or interactive effects of early-life WD and exercise. Our results demonstrate that both factors can have long-lasting effects on adult voluntary exercise and related phenotypes, and that these effects are modulated by genetic background. Overall, the long-lasting effects of early-life exercise were more pervasive than those of WD, suggesting critical opportunities for health intervention in childhood habits, as well as possible threats from modern challenges. These results may be relevant for understanding potential effects of activity reductions and dietary changes associated with the obesity epidemic and COVID-19 pandemic.

Early-life effects on body size in each sex interact to determine reproductive success in the burying beetle Nicrophorus vespilloides.

Early-life conditions have been shown to have a profound effect on an animal's body size and fecundity across diverse taxa. However, less is known about how early-life effects on fecundity within each sex interact to determine reproductive success. We used experiments with burying beetles Nicrophorus vespilloides to analyse this problem. The nutritional conditions experienced by burying beetles in early life are a key determinant of adult body size in both sexes, and adult body size in turn influences male reproductive tactics. In previous work, we showed that smaller males are more effective than larger males at stimulating virgin female fecundity. In this study, we manipulated male and female body size by restricting access to food in early development. We then conducted breeding assays, in which small and large females were mated sequentially with small and large males, and then allowed to raise offspring without paternal care. We tested whether large females, which are potentially more fecund, laid even more eggs when mated with small males. We found no evidence to support this prediction. Instead, we detected only a weak non-significant trend in the predicted direction and no equivalent trend in the number of larvae produced. However, we did find that larvae attained a greater mass by the end of development when their mother was large and mated with a small male first. We suggest that large females might have evolved counter-measures that prevent exploitation by small fecundity-stimulating males, including partial filial cannibalism. By eating surplus larvae during reproduction, larger females would leave more of the carrion for their offspring to consume. This could explain why their surviving larvae are able to attain a greater mass by the time they complete their development.

Illustrating the importance of meta-analysing variances alongside means in ecology and evolution.

Meta-analysis is increasingly used in biology to both quantitatively summarize available evidence for specific questions and generate new hypotheses. Although this powerful tool has mostly been deployed to study mean effects, there is untapped potential to study effects on (trait) variance. Here, we use a recently published data set as a case study to demonstrate how meta-analysis of variance can be used to provide insights into biological processes. This data set included 704 effect sizes from 89 studies, covering 56 animal species, and was originally used to test developmental stress effects on a range of traits. We found that developmental stress not only negatively affects mean trait values, but also increases trait variance, mostly in reproduction, showcasing how meta-analysis of variance can reveal previously overlooked effects. Furthermore, we show how meta-analysis of variance can be used as a tool to help meta-analysts make informed methodological decisions, even when the primary focus is on mean effects. We provide all data and comprehensive R scripts with detailed explanations to make it easier for researchers to conduct this type of analysis. We encourage meta-analysts in all disciplines to move beyond the world of means and start unravelling secrets of the world of variance.

Health effects of arsenic exposure in Latin America: An overview of the past eight years of research.

Studies conducted over the past eight years in Latin America (LA) have continued to produce new knowledge regarding health impacts of arsenic (As) in drinking water. We conducted a systematic review of 92 peer-reviewed English articles published between 2011 and 2018 to expand our understanding on these health effects. Majority of the LA studies on As have been conducted in Chile and Mexico. Additional data have emerged from As-exposed populations in Argentina, Bolivia, Brazil, Colombia, Ecuador, and Uruguay. The present review has documented recent data on the biomarkers of As exposure, genetic susceptibility and genotoxicity, and risk assessment to further characterize the health effects and exposed populations. Some recent findings on the associations of As with bladder and lung cancers, reproductive outcomes, and declined cognitive performance have been consistent with what we reported in our previous systematic review article. We have found highly convincing evidence of in utero As exposure as a significant risk factor for several health outcomes, particularly for bladder cancer, even at moderate level. New data have emerged regarding the associations of As with breast and laryngeal cancers as well as type 2 diabetes. We observed early life As exposure to be associated with kidney injury, carotid intima-media thickness, and various pulmonary outcomes in children. Other childhood effects such as low birth weight, low gestational age, anemia, increased apoptosis, and decreased cognitive functions were also reported. Studies identified genetic variants of As methyltransferase that could determine susceptibility to As related health outcomes. Arsenic-induced DNA damage and alteration of gene and protein expression have also been reported. While the scope of research is still vast, the substantial work done on As exposure and its health effects in LA will help direct further large-scale studies for more comprehensive knowledge and plan appropriate mitigation strategies.

Increased sperm production linked to competition in the maternal social environment.

Maternal or early life effects may prepare offspring for similar social conditions to those experienced by their mothers. For males, the ability to achieve mating and fertilization success is a key social challenge. Competitive conditions may therefore favour increased body size or ejaculate production in male offspring. We tested this experimentally by comparing reproductive traits of adult male bank voles (Myodes glareolus), whose mothers had experienced contrasting encounter regimes with female conspecifics while breeding. We found that daily sperm production rates and epididymis mass were significantly higher when dams had experienced more frequent encounters with female conspecifics. This response to maternal and early life experience was specific to sperm production and storage, with no evidence for effects on male body mass or the size of testes and accessory reproductive glands. Our findings reveal a potentially adaptive effect of maternal and early life experience on the development of sperm production, which is worthy of wider investigation.

Live long and prosper: durable benefits of early-life care in banded mongooses.

Kin selection theory defines the conditions for which altruism or 'helping' can be favoured by natural selection. Tests of this theory in cooperatively breeding animals have focused on the short-term benefits to the recipients of help, such as improved growth or survival to adulthood. However, research on early-life effects suggests that there may be more durable, lifelong fitness impacts to the recipients of help, which in theory should strengthen selection for helping. Here, we show in cooperatively breeding banded mongooses ( Mungos mungo) that care received in the first 3 months of life has lifelong fitness benefits for both male and female recipients. In this species, adult helpers called 'escorts' form exclusive one-to-one caring relationships with specific pups (not their own offspring), allowing us to isolate the effects of being escorted on later reproduction and survival. Pups that were more closely escorted were heavier at sexual maturity, which was associated with higher lifetime reproductive success for both sexes. Moreover, for female offspring, lifetime reproductive success increased with the level of escorting received per se, over and above any effect on body mass. Our results suggest that early-life social care has durable benefits to offspring of both sexes in this species. Given the well-established developmental effects of early-life care in laboratory animals and humans, we suggest that similar effects are likely to be widespread in social animals more generally. We discuss some of the implications of durable fitness benefits for the evolution of intergenerational helping in cooperative animal societies, including humans. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Early-life manipulation of cortisol and its receptor alters stress axis programming and social competence.

In many vertebrate species, early social experience generates long-term effects on later life social behaviour. These effects are accompanied by persistent modifications in the expression of genes implicated in the stress axis. It is unknown, however, whether stress axis programming can affect the development of social competence, and if so, by which mechanism(s). Here, we used pharmacological manipulations to persistently reprogramme the hypothalamic-pituitary-interrenal axis of juvenile cooperatively breeding cichlids, Neolamprologus pulcher. During the first two months of life, juveniles were repeatedly treated with cortisol, mifepristone or control treatments. Three months after the last manipulation, we tested for treatment effects on (i) social competence, (ii) the expression of genes coding for corticotropin-releasing factor ( crf), glucocorticoid receptor ( gr1) and mineralocorticoid receptor ( mr) in the telencephalon and hypothalamus and (iii) cortisol levels. Social competence in a social challenge was reduced in cortisol-treated juveniles, which is in accordance with previous work applying early-life manipulations using different social experiences. During early life, both cortisol and mifepristone treatments induced a persistent downregulation of crf and upregulation of mr in the telencephalon. We suggest that these persistent changes in stress gene expression may represent an effective physiological mechanism for coping with stress. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

A case for environmental statistics of early-life effects.

There is enduring debate over the question of which early-life effects are adaptive and which ones are not. Mathematical modelling shows that early-life effects can be adaptive in environments that have particular statistical properties, such as reliable cues to current conditions and high autocorrelation of environmental states. However, few empirical studies have measured these properties, leading to an impasse. Progress, therefore, depends on research that quantifies cue reliability and autocorrelation of environmental parameters in real environments. These statistics may be different for social and non-social aspects of the environment. In this paper, we summarize evolutionary models of early-life effects. Then, we discuss empirical data on environmental statistics from a range of disciplines. We highlight cases where data on environmental statistics have been used to test competing explanations of early-life effects. We conclude by providing guidelines for new data collection and reflections on future directions. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Making headway towards understanding how epigenetic mechanisms contribute to early-life effects.

It has become clear that in addition to the DNA sequence there is another layer of information, termed epigenetic modifications, that can influence phenotypes and traits. In particular, environmental epigenomics, which addresses the effect of the environment on the epigenome and human health, is becoming an area of great interest for many researchers working in different scientific fields. In this review, we will consider the current evidence that early-life environmental signals can have long-term effects on the epigenome. We will further evaluate how recent technological advances may enable us to unravel the molecular mechanisms underlying these phenomena, which will be crucial for understanding heritability in health and disease. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Preterm birth in evolutionary context: a predictive adaptive response?

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'.