The Demographic Transition Influences Variance in Fitness and Selection on Height and BMI in Rural Gambia

Abstract

SummaryRecent human history is marked by demographic transitions characterized by declines in mortality and fertility [1]. By influencing the variance in those fitness components, demographic transitions can affect selection on other traits [2]. 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 [3]. 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.

Understanding variation in human fertility: what can we learn from evolutionary demography?

“…Differential fertility may now be the primary engine of natural selection in postdemographic transition societies [156]. This raises the question of how best to measure fitness, since different measures can come up with different results (see [157,158] for an example of different measures of fitness resulting in exactly opposite conclusions using the same dataset). In this issue, Ewbank [159] highlights that reproductive timing matters (see also [160,161]), as failing to take into account the generational nature of reproduction may lead to the mismeasurement of fitness, particularly in humans and other long-lived organisms.…”

How does variance in fertility change over the demographic transition?

“…This approach to characterizing variance in fertility is different from other common approaches, in that it relies on linear rather than quadratic scaling between the mean and variance. For interested readers, we present results in the electronic supplementary material for other measures of variance of potential interest, including Crow's Index of Selection due to Fertility (Variance/Mean 2 ) [2,6] and the coefficient of variation (s.d./Mean) [10,11,42], which assume quadratic scaling between mean and variance.…”

“…In contrast to widely available data on mean fertility, much less is known about how other aspects of fertility distributions-most notably their variance-change as means decline [2][3][4]. Although the vast majority of demographic research has neglected changing variances in the study of fertility transitions, an evolutionary perspective demands attention to them [5][6][7].…”

“…Although the vast majority of demographic research has neglected changing variances in the study of fertility transitions, an evolutionary perspective demands attention to them [5][6][7]. Heritable variation is the raw material that natural selection works on, and efforts to estimate the heritability of fertility at different stages of the transition rely on the magnitude of phenotypic variance [2,3,[8][9][10][11][12][13]. The determinants of variance in fertility and reproductive skew is an active area in evolutionary theory in its own right [14][15][16].…”

When genes and environment disagree: Making sense of trends in recent human evolution

“…If the trait has some heritability and is associated with the number of children, researchers conclude that the traits are evolving as a result of natural selection (3). Height is highly heritable (4), so if taller individuals have more children, genes important for tall stature may become more frequent in future generations (5,6).…”