The adolescent transition under energetic stress: Body composition tradeoffs among adolescent women in The Gambia

Background and objectives: Life history theory predicts a shift in energy allocation from growth to reproductive function as a consequence of puberty. During adolescence, linear growth tapers off and, in females, ovarian steroid production increases. In this model, acquisition of lean mass is associated with growth while investment in adiposity is associated with reproduction. This study examines the chronological and developmental predictors of energy allocation patterns among adolescent women under conditions of energy constraint. Methodology: Fifty post-menarcheal adolescent women between 14 and 20 years old were sampled for weight and body composition at the beginning and end of 1 month in an energy-adequate season and 1 month in the subsequent energy-constrained season in a rural province of The Gambia. Results: Chronologically and developmentally younger adolescent girls gain weight in the form of lean mass in both energy-adequate and energy-constrained seasons, whereas older adolescents lose lean mass under conditions of energetic stress (generalized estimating equation (GEE) Wald chi-square comparing youngest tertile with older two tertiles 9.750, P = 0.002; GEE Wald chi-square comparing fastwith slow-growing individuals for growth rate 19.806, P< 0.001). When energy is limited, younger adolescents lose and older adolescents maintain fat (GEE Wald chi-square for interaction of age and season 6.568, P = 0.010; GEE Wald chi-square comparing fastwith slow-growing individuals for interaction of growth rate and season 7.807, P = 0.005). Conclusions and implications: When energy is constrained, the physiology of younger adolescents invests in growth while that of older adolescent females privileges reproductively valuable adipose tissue. K E Y W O R D S : life history theory; puberty; body composition; reproductive ecology original research article 75 The Author(s) 2013. Published by Oxford University Press on behalf of the Foundation for Evolution, Medicine, and Public Health. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. BACKGROUND AND OBJECTIVES Puberty is the transition from non-reproductive juvenility to reproductively capable maturity. In the terms of life history theory [1], puberty represents a transition in energy allocation: during the juvenile period, energy available beyond the requirements of maintenance is used for growth, as demonstrated by accelerated growth rates in well-nourished populations relative to energy-constrained populations [2]. At puberty, this surplus energy begins to be invested in reproductive function [3]. For human females, reproductive function is reflected by ovarian steroid production. Ovarian estradiol promotes the conversion of energy into adipose tissue [4], which is mobilized during gestation and lactation [5]. In the adolescent female body, therefore, acquisition of lean mass, comprising bones, muscle, water and organs, equates, in life history terms, to investment in growth, while acquisition or preferential maintenance of adipose tissue can be understood as investment in reproduction. Although puberty itself begins with a specific endocrine event, the initiation of pulsatile gonadotropin releasing hormone (GnRH) secretion from the arcuate nucleus of the hypothalamus [6, 7], the transition from juvenility to maturity occurs over the course of several years (Supplementary Fig. S1). Linear growth continues during this time, with height velocity in females generally peaking a year prior to menarche [8]. The overlap of these two phenomena, the adolescent linear height spurt and the externally visible sign of maturing gonadal function, indicates that adolescent physiology must allocate energy simultaneously to growth and reproductive function. This functional overlap is in keeping with the constrained fecundity seen in the years immediately after menarche, a phenomenon often referred to as ‘adolescent sterility’ but more accurately termed ‘adolescent subfecundity’ [9, 10]. The role of energy availability in mediating the timing of pubertal maturation in traditional and industrialized populations has been documented: while a high ratio of adult to juvenile extrinsic mortality risk promotes early age at maturity even when energy is limited [11, 12], there is generally a negative relationship between energy availability and juvenile growth rates on the one hand and age at puberty on the other hand [2]. Less is known, however, about the determinants of somatic energy allocation during puberty. This is a particularly relevant question for females, for whom a single reproductive event equates to 300 average kilocalories per day for the 9 months of gestation (calculated with the equation from Aiello and Key [13] for a 42.2 kg !Kung woman) and 640 kcal per day for 6 months of lactation [14]. At the same time, adiposity is not the only somatic reproductive asset in women: in some developing world populations, female height correlates positively with marriageability and with reproductive success [15–17], suggesting that somatic investments in linear growth—or in one of its correlates, such as pelvic growth—may yield reproductive dividends. It is important to keep in mind, however, that greater height may indicate that growth has already ceased and the individual is prepared to invest in reproduction. This study investigated the determinants of somatic allocation strategy in energetically constrained adolescent women, many of whom have not completed linear growth. We asked the question: What developmental and chronological markers predict the transition from preferential investment in growth in the form of lean mass to investment in reproduction in the form of fat mass? We predicted that, in an energetically constrained population of adolescent women in The Gambia, developmental age would predict somatic energy allocation strategy. The answer to this question will contribute to our understanding of what constitutes evolutionarily relevant cues to modulating the tempo of reproductive maturation in females.