Environmental Quality, Developmental Plasticity and the Thrifty Phenotype: A Review of Evolutionary Models

The concept of the thrifty phenotype, first proposed by Hales and Barker, is now widely used in medical research, often in contrast to the thrifty genotype model, to interpret associations between early-life experience and adult health status. Several evolutionary models of the thrifty phenotype, which refers to developmental plasticity, have been presented. These include (A) the weather forecast model of Bateson, (B) the maternal fitness model of Wells, (C) the intergenerational phenotypic inertia model of Kuzawa, and (D) the predictive adaptive response model of Gluckman and Hanson. These models are compared and contrasted, in order to assess their relative utility for understanding human ontogenetic development. The most broadly applicable model is model A, which proposes that developing organisms respond to cues of environmental quality, and that mismatches between this forecast and subsequent reality generate significant adverse effects in adult phenotype. The remaining models all address in greater detail what kind of information is provided by such a forecast. Whereas both models B and C emphasise the adaptive benefits of exploiting information about the past, encapsulated in maternal phenotype, model D assumes that the fetus uses cues about the present external environment to predict its probable adult environment. I argue that for humans, with a disproportionately long period between the closing of sensitive windows of plasticity and the attainment of reproductive maturity, backward-looking models B and C represent a better approach, and indicate that the developing offspring aligns itself with stable cues of maternal phenotype so as to match its energy demand with maternal capacity to supply. In contrast, the predictive adaptive response model D over-estimates the capacity of the offspring to predict the future, and also fails to address the long-term parent-offspring dynamics of human development. Differences between models have implications for the design of public health interventions

Natural selection and human adiposity: crafty genotype, thrifty phenotype

Evolutionary perspectives on obesity have aimed to understand how the genetic constitution of individuals has been shaped by selective pressures such as famine, predation or infectious disease. The dual intervention model assumes strong selection on lower and upper limits of adiposity, but negligible fitness implications for intermediate adiposity. These frameworks are agnostic to age, sex and condition. I argue that selection has favoured a 'crafty genotype'-a genetic basis for accommodating variability in the 'fitness value' of fat through phenotypic plasticity, depending on the endogenous and exogenous characteristics of each individual. Hominin evolution occurred in volatile environments. I argue that the polygenetic basis of adiposity stabilizes phenotype in such environments, while also coordinating phenotypic variance across traits. This stability underpins reaction norms through which adiposity can respond sensitively to ecological factors. I consider how the fitness value of fat changes with age, sex and developmental experience. Fat is also differentially distributed between peripheral and abdominal depots, reflecting variable prioritization of survival versus reproduction. Where longevity has been compromised by undernutrition, abdominal fat may promote immediate survival and fitness, while long-term cardiometabolic risks may never materialize. This approach helps understand the sensitivity of adiposity to diverse environmental factors, and why the health impacts of obesity are variable. This article is part of a discussion meeting issue 'Causes of obesity: theories, conjectures and evidence (Part I)'

An evolutionary perspective on social inequality and health disparities: Insights from the producer–scrounger game

There is growing concern with social disparities in health, whether relating to gender, ethnicity, caste, socio-economic position or other axes of inequality. Despite addressing inequality, evolutionary biologists have had surprisingly little to say on why human societies are prone to demonstrating exploitation. This article builds on a recent book, 'The Metabolic Ghetto', describing an overarching evolutionary framework for studying all forms of social inequality involving exploitation. The dynamic 'producer-scrounger' game, developed to model social foraging, assumes that some members of a social group produce food, and that others scrounge from them. An evolutionary stable strategy emerges when neither producers nor scroungers can increase their Darwinian fitness by changing strategy. This approach puts food systems central to all forms of human inequality, and provides a valuable lens through which to consider different forms of gender inequality, socio-economic inequality and racial/caste discrimination. Individuals that routinely adopt producer or scrounger tactics may develop divergent phenotypes. This approach can be linked with life history theory to understand how social dynamics drive health disparities. The framework differs from previous evolutionary perspectives on inequality, by focussing on the exploitation of foraging effort rather than inequality in ecological resources themselves. Health inequalities emerge where scroungers acquire different forms of power over producers, driving increasing exploitation. In racialized societies, symbolic categorization is used to systematically assign some individuals to low-rank producer roles, embedding exploitation in society. Efforts to reduce health inequalities must address the whole of society, altering producer-scrounger dynamics rather than simply targeting resources at exploited groups

An Evolutionary Model of "Sexual Conflict" Over Women's Age at Marriage: Implications for Child Mortality and Undernutrition

Background: Early women's marriage is associated with adverse outcomes for mothers and their offspring, including reduced human capital and increased child undernutrition and mortality. Despite preventive efforts, it remains common in many populations and is often favored by cultural norms. A key question is why it remains common, given such penalties. Using an evolutionary perspective, a simple mathematical model was developed to explore women's optimal marriage age under different circumstances, if the sole aim were to maximize maternal or paternal lifetime reproductive fitness (surviving offspring). Methods: The model was based on several assumptions, supported by empirical evidence, regarding relationships between women's marital age and parental and offspring outcomes. It assumes that later marriage promotes women's autonomy, enhancing control over fertility and childcare, but increases paternity uncertainty. Given these assumptions, optimal marriage ages for maximizing maternal and paternal fitness were calculated. The basic model was then used to simulate environmental changes or public health interventions, including shifts in child mortality, suppression of women's autonomy, or promoting women's contraception or education. Results: In the basic model, paternal fitness is maximized at lower women's marriage age than is maternal fitness, with the paternal optimum worsening child undernutrition and mortality. A family planning intervention delays marriage age and reduces child mortality and undernutrition, at a cost to paternal but not maternal fitness. Reductions in child mortality favor earlier marriage but increase child undernutrition, whereas ecological shocks that increase child mortality favor later marriage but reduce fitness of both parents. An education intervention favors later marriage and reduces child mortality and undernutrition, but at a cost to paternal fitness. Efforts to suppress maternal autonomy substantially increase fitness of both parents, but only if other members of the household provide compensatory childcare. Conclusion: Early women's marriage maximizes paternal fitness despite relatively high child mortality and undernutrition, by increasing fertility and reducing paternity uncertainty. This tension between the sexes over the optimal marriage age is sensitive to ecological stresses or interventions. Education interventions seem most likely to improve maternal and child outcomes, but may be resisted by males and their kin as they may reduce paternal fitness

Maternal capital predicts investment in infant growth and development through lactation

INTRODUCTION: Maternal capital (MC) is a broad term from evolutionary biology, referring to any aspects of maternal phenotype that represent resources available for investment in offspring. We investigated MC in breastfeeding mothers of late preterm and early term infants, examining its relationship with infant and breastfeeding outcomes. We also determined whether MC modified the effect of the relaxation intervention on these outcomes. METHODS: The data was collected as part of a randomized controlled trial investigating breastfeeding relaxation in 72 mothers of late preterm and early term infants. Indicators of MC (socioeconomic, social, somatic, reproductive, psychological, and cognitive) were collected at baseline at 2-3 weeks post-delivery. Principal Component Analysis was conducted for the MC measures and two components were identified: 1."Subjective" maternal capital which included stress and depression scores, and 2."Objective" maternal capital which included height, infant birth weight, and verbal memory. Univariate linear regression was conducted to assess the relationship between objective and subjective MC (predictors) and infant growth, infant behavior, maternal behavior, and infant feeding variables (outcomes) at 6-8 weeks. The interaction of MC and intervention assignment with outcomes was assessed. RESULTS: Higher objective MC was significantly associated with higher infant weight (0.43; 95%CI 0.21,0.66) and length z-scores (0.47; 95%CI 0.19,0.76), shorter duration of crying (-17.5; 95%CI -33.2,-1.9), and lower food (-0.28; 95%CI -0.48,-0.08) and satiety responsiveness (-0.17; 95%CI -0.31,-0.02) at 6-8 weeks. It was also associated with greater maternal responsiveness to infant cues (-0.05, 95%CI -0.09,-0.02 for non-responsiveness). Greater subjective maternal capital was significantly associated with higher breastfeeding frequency (2.3; 95%CI 0.8,3.8) and infant appetite (0.30; 95%CI 0.07,0.54). There was a significant interaction between the intervention assignment and objective MC for infant length, with trends for infant weight and crying, which indicated that the intervention had greater effects among mothers with lower capital. CONCLUSION: Higher MC was associated with better infant growth and shorter crying duration. This was possibly mediated through more frequent breastfeeding and prompt responsiveness to infant cues, reflecting greater maternal investment. The findings also suggest that a relaxation intervention was most effective among those with low MC, suggesting some reduction in social inequalities in health

Population history and ecology, in addition to climate, influence human stature and body proportions.

Worldwide variation in human stature and limb proportions is widely accepted to reflect thermal adaptation, but the contribution of population history to this variation is unknown. Furthermore, stature and relative lower limb length (LLL) show substantial plastic responses to environmental stressors, e.g., nutrition, pathogen load, which covary with climate. Thus ecogeographic patterns may go beyond temperature-based selection. We analysed global variation in stature, sitting height and absolute and relative LLL using large worldwide samples of published anthropometric data from adult male (n = 571) and female (n = 268) populations in relation to temperature, humidity, and net primary productivity (NPP). Population history was modeled using spatial eigenvector mapping based on geographic distances reflecting the hypothesized pattern for the spread of modern humans out of Africa. Regression models account for ~ 50% of variation in most morphological variables. Population history explains slightly more variation in stature, sitting height and LLL than the environmental/climatic variables. After adjusting for population history, associations between (usually maximum) temperature and LLL are consistent with Allen's "rule" and may drive similar relationships with stature. NPP is a consistent negative predictor of anthropometry, which may reflect the growth-limiting effects of lower environmental resource accessibility (inversely related to NPP) and/or pathogen load

Reconsidering the developmental origins of adult disease paradigm: the ‘metabolic coordination of childbirth’ hypothesis

In uncomplicated pregnancies, birthweight is inversely associated with adult non-communicable disease (NCD) risk. One proposed mechanism is maternal malnutrition during pregnancy. Another explanation is that shared genes link birthweight with NCDs. Both hypotheses are supported, but evolutionary perspectives address only the environmental pathway. We propose that genetic and environmental associations of birthweight with NCD risk reflect coordinated regulatory systems between mother and fetus, that evolved to reduce risks of obstructed labour. First, the fetus must tailor its growth to maternal metabolic signals, as it cannot predict the size of the birth canal from its own genome. Second, we predict that maternal alleles that promote placental nutrient supply have been selected to constrain fetal growth and gestation length when fetally expressed. Conversely, maternal alleles that increase birth canal size have been selected to promote fetal growth and gestation when fetally expressed. Evidence supports these hypotheses. These regulatory mechanisms may have undergone powerful selection as hominin neonates evolved larger size and encephalisation, since every mother is at risk of gestating a baby excessive for her pelvis. Our perspective can explain the inverse association of birthweight with NCD risk across most of the birthweight range: any constraint of birthweight, through plastic or genetic mechanisms, may reduce the capacity for homeostasis and increase NCD susceptibility. However, maternal obesity and diabetes can overwhelm this coordination system, challenging vaginal delivery while increasing offspring NCD risk. We argue that selection on viable vaginal delivery played an over-arching role in shaping the association of birthweight with NCD risk