Natural selection and human adiposity: crafty genotype, thrifty phenotype

Abstract

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)'.

Keywords: adiposity; evolution; fat distribution; infectious disease; phenotypic plasticity; reaction norm.

Figure 1.

Schematic diagram illustrating the fitness functions of adipose tissue, and their exposure through human behaviour to the selective pressure of colonizing novel environments. (Online version in colour.)

Figure 2.

Schematic diagram illustrating how alleles associated with energy stores (adiposity alleles) relate to diverse physiological functions. The relative importance of these functions may vary through the life-course in both systematic ways (age, sex), and individual ways depending on the exposures experienced. (Online version in colour.)

Figure 3.

Age and sex variability in human body composition. (a) Fat mass index plotted against fat-free mass index from birth to 18 years, using the 50th centile of UK reference data [64,65]. Fatness is high in infancy, then declines before increasing again in mid-childhood, though with increasing sexual dimorphism. (b) Variability in fat distribution in Thai women. Residuals from regressing waist girth on BMI, and thigh girth on hip girth, are plotted against age group for parous and non-parous women. In both groups, waist-BMI increases and thigh–hip declines with age, indicating redistribution of body fat, though the data are cross-sectional. Data from the National Sizing Survey of Thailand. Redrawn with permission [78]. (Online version in colour.)