Intergenerational capital flows are central to fitness dynamics and adaptive evolution in humans.

Human fitness dynamics are uniquely and profoundly governed by the flow of capital to subsequent generations. Low socioeconomic status individuals may possess limited capacity to direct capital to descendants and may respond to such constraints adaptively or maladaptively. Mitigation of capital constraints may provide practicable routes to alleviation of the behavioural constellation of deprivation.

Genetic Associations Between Personality Traits and Lifetime Reproductive Success in Humans.

Personality has been associated with reproductive success in humans and other animals, suggesting potential evolutionary selection pressures. However, studies to date have only examined these associations on a phenotypic level, which may be inadequate in estimating evolutionary change. Using a large longitudinal twin dataset of contemporary Finns, we compared the phenotypic (breeder's equation) and genetically informed (the Robertson-Price identity) associations between lifetime reproductive success (LRS) and two personality traits-neuroticism and extraversion. Neuroticism was not associated with LRS at the phenotypic nor genetic level, while extraversion was associated with higher LRS in men both phenotypically and genetically. Compared to the univariate phenotypic analysis, the genetic analysis suggested a larger selection response of extraversion, and a selection response of neuroticism due to indirect selection. We estimated that neuroticism decreases by .05 standard deviations and extraversion increases by .11 standard deviations by one generation. Our results highlight the importance of considering genetic associations between personality and fitness and investigating several inter-related personality traits and their covariance with each other to predict responses to selection more accurately.

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.

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.

Intergenerational effects of maternal birth season on offspring size in rural Gambia.

Environmental conditions experienced in early life can influence an individual's growth and long-term health, and potentially also that of their offspring. However, such developmental effects on intergenerational outcomes have rarely been studied. Here we investigate intergenerational effects of early environment in humans using survey- and clinic-based data from rural Gambia, a population experiencing substantial seasonal stress that influences foetal growth and has long-term effects on first-generation survival. Using Fourier regression to model seasonality, we test whether (i) parental birth season has intergenerational consequences for offspring in utero growth (1982 neonates, born 1976-2009) and (ii) whether such effects have been reduced by improvements to population health in recent decades. Contrary to our predictions, we show effects of maternal birth season on offspring birth weight and head circumference only in recent maternal cohorts born after 1975. Offspring birth weight varied according to maternal birth season from 2.85 to 3.03 kg among women born during 1975-1984 and from 2.84 to 3.41 kg among those born after 1984, but the seasonality effect reversed between these cohorts. These results were not mediated by differences in maternal age or parity. Equivalent patterns were observed for offspring head circumference (statistically significant) and length (not significant), but not for ponderal index. No relationships were found between paternal birth season and offspring neonatal anthropometrics. Our results indicate that even in rural populations living under conditions of relative affluence, brief variation in environmental conditions during maternal early life may exert long-term intergenerational effects on offspring.

Twinning propensity and offspring in utero growth covary in rural African women.

In humans and other mammals, some females are more likely to experience twin pregnancies than others, but the reasons behind such individual variation are poorly understood. One hypothesis invokes variation in the dynamics of the insulin-like growth factor (IGF) system, which also regulates foetal growth. Using data from a rural African population living in a highly seasonal environment, we test a novel prediction generated by this hypothesis, that maternal twinning status predicts offspring birthweight. We found that among singleton offspring who experience a favourable in utero environment (born January-June), births before and after twins are, respectively, associated with a 134.07 g and 226.41 g increase in birthweight compared with those born to non-twinning mothers. These results were not mediated by maternal anthropometry. This is consistent with a role for the IGF system in individual variation in twinning propensity, a possibility with implications for understanding mechanisms of life-history variation in humans and other vertebrates.

Serum IGF-I in middle age covaries with reproductive life-history traits in British men and women.

OBJECTIVES: The growth hormone/insulin-like growth factor-I (GH/IGF-I) axis may be an important component of individual life-history variation. This study examined whether IGF-I levels covary with reproductive life-history traits in a long-term British cohort study (the National Child Development Study). METHODS: Using data on up to 5,252 individuals (2,431 men and 2,821 women) born in March 1958, relationships of serum IGF-I at age 45 with pubertal age, time to pregnancy (TTP), age at first reproduction (AFR), and lifetime reproductive success (LRS) were analyzed using general linear models. RESULTS: IGF-I showed modest non-linear associations with pubertal age, being low in women who first menstruated, and men whose voice broke, in the oldest respective age categories. In women, but not men, IGF-I was negatively related to TTP. IGF-I was positively associated with AFR in both sexes and tended to be negatively related to LRS in women only. Some, but not all, relationships were attenuated after controlling for multiple potential confounders. CONCLUSION: These results are consistent with the hypothesis that the GH/IGF-I axis partially underlies individual variance in reproductive outcomes, through either direct endocrine effects on reproductive function or behavior, indirect effects on other traits, or a combination of the above. Several limitations of this study include the late age at which blood samples were collected and the difficulty of disentangling social and biological factors contributing to the traits studied. Am. J. Hum. Biol., 2012. © 2012 Wiley Periodicals, Inc.

Mothers with higher twinning propensity had lower fertility in pre-industrial Europe.

Historically, mothers producing twins gave birth, on average, more often than non-twinners. This observation has been interpreted as twinners having higher intrinsic fertility - a tendency to conceive easily irrespective of age and other factors - which has shaped both hypotheses about why twinning persists and varies across populations, and the design of medical studies on female fertility. Here we show in >20k pre-industrial European mothers that this interpretation results from an ecological fallacy: twinners had more births not due to higher intrinsic fertility, but because mothers that gave birth more accumulated more opportunities to produce twins. Controlling for variation in the exposure to the risk of twinning reveals that mothers with higher twinning propensity - a physiological predisposition to producing twins - had fewer births, and when twin mortality was high, fewer offspring reaching adulthood. Twinning rates may thus be driven by variation in its mortality costs, rather than variation in intrinsic fertility.

Food availability at birth limited reproductive success in historical humans.

Environmental conditions in early life can profoundly affect individual development and have consequences for reproductive success. Limited food availability may be one of the reasons for this, but direct evidence linking variation in early-life nutrition to reproductive performance in adulthood in natural populations is sparse. We combined historical agricultural data with detailed demographic church records to investigate the effect of food availability around the time of birth on the reproductive success of 927 men and women born in 18th-century Finland. Our study population exhibits natural mortality and fertility rates typical of many preindustrial societies, and individuals experienced differing access to resources due to social stratification. We found that among both men and women born into landless families (i.e., with low access to resources), marital prospects, probability of reproduction, and offspring viability were all positively related to local crop yield during the birth year. Such effects were generally absent among those born into landowning families. Among landless individuals born when yields of the two main crops, rye and barley, were both below median, only 50% of adult males and 55% of adult females gained any reproductive success in their lifetime, whereas 97% and 95% of those born when both yields were above the median did so. Our results suggest that maternal investment in offspring in prenatal or early postnatal life may have profound implications for the evolutionary fitness of human offspring, particularly among those for which resources are more limiting. Our study adds support to the idea that early nutrition can limit reproductive success in natural animal populations, and provides the most direct evidence to date that this process applies to humans.

The predictive adaptive response and metabolic syndrome: challenges for the hypothesis.

In humans and other mammals, maternal undernutrition or stress during gestation results in small offspring with permanently altered metabolism and tissue composition. It has been suggested that such responses might exist because in utero conditions provide a reliable 'prediction' of the environmental conditions that foetuses will eventually be exposed to during adulthood. Thus, some developmental responses to the early environment might improve an individual's evolutionary success in a similar future environment.

Producing sons reduces lifetime reproductive success of subsequent offspring in pre-industrial Finns.

Life-history theory states that reproductive events confer costs upon mothers. Many studies have shown that reproduction causes a decline in maternal condition, survival or success in subsequent reproductive events. However, little attention has been given to the prospect of reproductive costs being passed onto subsequent offspring, despite the fact that parental fitness is a function of the reproductive success of progeny. Here we use pedigree data from a pre-industrial human population to compare offspring life-history traits and lifetime reproductive success (LRS) according to the cost incurred by each individual's mother in the previous reproductive event. Because producing a son versus a daughter has been associated with greater maternal reproductive cost, we hypothesize that individuals born to mothers who previously produced sons will display compromised survival and/or LRS, when compared with those produced following daughters. Controlling for confounding factors such as socio-economic status and ecological conditions, we show that those offspring born after elder brothers have similar survival but lower LRS compared with those born after elder sisters. Our results demonstrate a maternal cost of reproduction manifested in reduced LRS of subsequent offspring. To our knowledge, this is the first time such a long-term intergenerational cost has been shown in a mammal species.

Why Are Childhood Family Factors Associated With Timing of Maturation? A Role for Internal Prediction.

Children, particularly girls, who experience early familial adversity tend to go on to reach sexual maturity relatively early. This feature of adolescent development is believed to be an evolved strategy that arose because individuals with genes that caused them to mature relatively early under certain conditions left behind more descendants than those who did not. However, although much has been done to uncover the psychological and physiological mechanisms underlying this process, less attention has been paid to the evolutionary reasons behind why it might be advantageous. It has previously been suggested that this strategy evolved because early familial adversity accurately indicated later environmental adversity, under which conditions early reproduction would likely maximize evolutionary fitness. In this article, we contrast this "external prediction" model with an alternative explanation, which builds on the existing explanation and is mutually compatible with it but also distinct from it. We argue that accelerated development is advantageous because early adversity detrimentally affects the individual's body, increasing later morbidity and mortality; individuals may adapt to this internal setback by accelerating their development. Unlike the external prediction model, this "internal prediction" relies not on temporal environmental continuity but on long-term effects of early circumstances on the body.

What can cross-cultural correlations teach us about human nature?

Many recent evolutionary psychology and human behavioral ecology studies have tested hypotheses by examining correlations between variables measured at a group level (e.g., state, country, continent). In such analyses, variables collected for each aggregation are often taken to be representative of the individuals present within them, and relationships between such variables are presumed to reflect individual-level processes. There are multiple reasons to exercise caution when doing so, including: (1) the ecological fallacy, whereby relationships observed at the aggregate level do not accurately represent individual-level processes; (2) non-independence of data points, which violates assumptions of the inferential techniques used in null hypothesis testing; and (3) cross-cultural non-equivalence of measurement (differences in construct validity between groups). We provide examples of how each of these gives rise to problems in the context of testing evolutionary hypotheses about human behavior, and we offer some suggestions for future research.

The demographic transition influences variance in fitness and selection on height and BMI in rural Gambia.

Recent human history is marked by demographic transitions characterized by declines in mortality and fertility. By influencing the variance in those fitness components, demographic transitions can affect selection on other traits. Parallel to changes in selection triggered by demography per se, relationships between fitness and anthropometric traits are also expected to change due to modification of the environment. Here we explore for the first time these two main evolutionary consequences of demographic transitions using a unique data set containing survival, fertility, and anthropometric data for thousands of women in rural Gambia from 1956-2010. We show how the demographic transition influenced directional selection on height and body mass index (BMI). We observed a change in selection for both traits mediated by variation in fertility: selection initially favored short females with high BMI values but shifted across the demographic transition to favor tall females with low BMI values. We demonstrate that these differences resulted both from changes in fitness variance that shape the strength of selection and from shifts in selective pressures triggered by environmental changes. These results suggest that demographic and environmental trends encountered by current human populations worldwide are likely to modify, but not stop, natural selection in humans.

The adaptive basis of psychosocial acceleration: comment on Beyond Mental Health, Life History Strategies articles.

Four of the articles published in this special section of Developmental Psychology build on and refine psychosocial acceleration theory. In this short commentary, we discuss some of the adaptive assumptions of psychosocial acceleration theory that have not received much attention. Psychosocial acceleration theory relies on the behavior of caregivers being a reliable cue of broader ecological conditions and on those ecological conditions being somewhat stable over the individual's lifetime. There is a scope for empirical and theoretical work investigating the range of environments over which these assumptions hold, to understand more deeply why it is that early life family environment exerts such reliable effects on later life-history strategy.