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Tradeoffs between immune function and childhood growth among Amazonian forager-horticulturalists

S. Urlacher,P. Ellison,L. Sugiyama,Herman Pontzer,Herman Pontzer,G. Eick,M. Liebert,T. Cepon‐Robins,T. Gildner,J. Snodgrass

Published 2018 in Proceedings of the National Academy of Sciences of the United States of America

ABSTRACT

Significance The energetic impact of immune function on human growth remains unclear. Using data from Amazonian forager-horticulturalists, we show that diverse, low-level immune activity predicts reduced childhood growth over periods of competing energy use ranging from 1 wk to 20 mo. We also demonstrate that modest body fat stores (i.e., energy reserves) protect children from the particularly detrimental impact of acute inflammation on growth. These findings provide evidence for considerable energetic tradeoffs between immune function and growth among humans, highlighting the energy constraint of childhood and the characteristic ability of our species to respond sensitively to dynamic environmental conditions. We outline the possible role of immune-related tradeoffs in driving patterns of human growth faltering, developmental metabolic plasticity, and life history evolution. Immune function is an energetically costly physiological activity that potentially diverts calories away from less immediately essential life tasks. Among developing organisms, the allocation of energy toward immune function may lead to tradeoffs with physical growth, particularly in high-pathogen, low-resource environments. The present study tests this hypothesis across diverse timeframes, branches of immunity, and conditions of energy availability among humans. Using a prospective mixed-longitudinal design, we collected anthropometric and blood immune biomarker data from 261 Amazonian forager-horticulturalist Shuar children (age 4–11 y old). This strategy provided baseline measures of participant stature, s.c. body fat, and humoral and cell-mediated immune activity as well as subsample longitudinal measures of linear growth (1 wk, 3 mo, 20 mo) and acute inflammation. Multilevel analyses demonstrate consistent negative effects of immune function on growth, with children experiencing up to 49% growth reduction during periods of mildly elevated immune activity. The direct energetic nature of these relationships is indicated by (i) the manifestation of biomarker-specific negative immune effects only when examining growth over timeframes capturing active competition for energetic resources, (ii) the exaggerated impact of particularly costly inflammation on growth, and (iii) the ability of children with greater levels of body fat (i.e., energy reserves) to completely avoid the growth-inhibiting effects of acute inflammation. These findings provide evidence for immunologically and temporally diverse body fat-dependent tradeoffs between immune function and growth during childhood. We discuss the implications of this work for understanding human developmental energetics and the biological mechanisms regulating variation in human ontogeny, life history, and health.

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