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

Abstract

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.

Can environmental conditions experienced in early life influence future generations?

“…For example, several longitudinal analyses of human populations revealed that conditions during an F 0 mother's pregnancy could alter the birth characteristics and/or later-life health of her F 2 grandchildren [11–13]. However, such effects are not necessarily restricted to the maternal lineage nor first generation offspring: decreased lifespan has been reported in men whose paternal grandfather experienced poor nutrition during childhood [14].…”

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

“…producing smaller neonates with lower survival prospects (Rickard et al, 2012)), but 108 gaining an advantage of earlier reproduction (e.g., offsetting the risk of dying herself 109 before becoming reproductively successful). The optimal age for a female to become 110 sexually mature changes as the costs and benefits of starting to reproduce early 111 relative to delaying alter.…”

“…Selection for this efficiency leads to trade-offs between different 104 activities that can ultimately serve that purpose. When a female becomes sexually 105 mature, she is potentially diverting resources away from her own growth towards 106 reproduction, disadvantaging herself and her offspring in some respects (e.g., 107producing smaller neonates with lower survival prospects (Rickard et al, 2012)), but 108 gaining an advantage of earlier reproduction (e.g., offsetting the risk of dying herself 109 before becoming reproductively successful). The optimal age for a female to become 110 sexually mature changes as the costs and benefits of starting to reproduce early 111 relative to delaying alter.…”

Transgenerational Impact of Nutrition on Disease Risk

“…A recent study in the Gambia showed that brief variations of the environmental conditions in mothers' own early life have long-term transgenerational effects on offspring's size at birth (Rickard et al, 2012). In the Gambia, there are large seasonal variations in food supply.…”

“…These increased death rates have been shown to be mainly due to infectious disease (Moore et al, 2004). Recently, the first evidence was published to suggest that maternal but not paternal season of birth was associated with offspring's birth weight and head circumference (Rickard et al, 2012). The authors concluded, ''The persistence of these relationships when controlling for measures of maternal size indicate that the mechanisms behind intergenerational effects of maternal early conditions may not be found in a simple model of maternal physical or physiological constraint and point to the need to account for other aspects of maternal phenotype associated with offspring growth such as pelvic dimensions, physiological parameters like insulin metabolism, glucocorticoid levels, hypertension or epigenetic inheritance''.…”