Abstract

BackgroundAverage profiles of salivary progesterone in women vary significantly at the inter- and intrapopulation level as a function of age and acute energetic conditions related to energy intake, energy expenditure, or a combination of both. In addition to acute stressors, baseline progesterone levels differ among populations. The causes of such chronic differences are not well understood, but it has been hypothesised that they may result from varying tempos of growth and maturation and, by implication, from diverse environmental conditions encountered during childhood and adolescence.Methods and FindingsTo test this hypothesis, we conducted a migrant study among first- and second-generation Bangladeshi women aged 19–39 who migrated to London, UK at different points in the life-course, women still resident in Bangladesh, and women of European descent living in neighbourhoods similar to those of the migrants in London (total n = 227). Data collected included saliva samples for radioimmunoassay of progesterone, anthropometrics, and information from questionnaires on diet, lifestyle, and health. Results from multiple linear regression, controlled for anthropometric and reproductive variables, show that women who spend their childhood in conditions of low energy expenditure, stable energy intake, good sanitation, low immune challenges, and good health care in the UK have up to 103% higher levels of salivary progesterone and an earlier maturation than women who develop in less optimal conditions in Sylhet, Bangladesh (F 9,178 = 5.05, p < 0.001, standard error of the mean = 0.32; adjusted R 2 = 0.16). Our results point to the period prior to puberty as a sensitive phase when changes in environmental conditions positively impact developmental tempos such as menarcheal age (F 2,81 = 3.21, p = 0.03) and patterns of ovarian function as measured using salivary progesterone (F 2,81 = 3.14, p = 0.04).ConclusionsThis research demonstrates that human females use an extended period of the life cycle prior to reproductive maturation to monitor their environment and to modulate reproductive steroid levels in accordance with projected conditions they might encounter as adults. Given the prolonged investment of human pregnancy and lactation, such plasticity (extending beyond any intrauterine programming) enables a more flexible and finely tuned adjustment to the potential constraints or opportunities of the later adult environment. This research is the first, to our knowledge, to demonstrate a postuterine developmental component to variation in reproductive steroid levels in women.

Highlights

  • For the past two decades, innovative methods for monitoring ovarian function have encouraged the detailed study of human reproductive function among genetically, culturally, and ecologically diverse populations in field settings

  • In addition to acute stressors, baseline progesterone levels differ among populations. The causes of such chronic differences are not well understood, but it has been hypothesised that they may result from varying tempos of growth and maturation and, by implication, from diverse environmental conditions encountered during childhood and adolescence

  • Age at migration was significantly correlated with menarcheal age (r 1⁄4 0.31, p 1⁄4 0.03, n 1⁄4 39)

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Summary

Introduction

For the past two decades, innovative methods for monitoring ovarian function have encouraged the detailed study of human reproductive function among genetically, culturally, and ecologically diverse populations in field settings. Women’s reproductive biology—which includes levels of sex hormones at different stages of the menstrual cycle—is known to vary greatly depending on the environment This variation can be measured by looking at the levels of certain reproductive hormones in the saliva, for example, progesterone and estradiol. Women who live in environments where less food is available or infections are more common, or who do more physical work seem to have lower levels of these hormones compared to other women Because these differences seem to persist over the long term, some researchers have suggested that various factors relating to an individual’s environment early in life have a strong influence on later fertility. The logical basis for this idea is attractive, there is not very much evidence that it is true

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