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

Abstract

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 () the manifestation of biomarker-specific negative immune effects only when examining growth over timeframes capturing active competition for energetic resources, () the exaggerated impact of particularly costly inflammation on growth, and () 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.

Soil‐transmitted helminth infection and intestinal inflammation among the Shuar of Amazonian Ecuador

“…An alternative explanation may be that the generally high bacterial and viral pathogen environment, poor sanitation, and high degree of fecal-oral contamination are elevating localized intestinal inflammation among Shuar children as their primary immune response switches from the proinflammatory innate response to the more regulated, anti-inflammatory adaptive response (Blackwell et al, 2010(Blackwell et al, , 2011. In this case, we hypothesize that the high pathogen environment documented among the Shuar (Stagaman et al, 2018;Urlacher et al, 2018) may play a role in childhood rates of elevated inflammation in this sample. It is possible that we would see lower rates of elevated intestinal inflammation among Shuar children from more market-integrated regions with better sanitation and reduced bacterial and viral pathogen exposure.…”

“…Inflammatory and infectious disease patterns are deeply interwoven with body composition and nutritional status (McDade, 2012;Urlacher et al, 2016Urlacher et al, , 2018 and, because of this small sample size, we cannot speak to their effects here. Inflammatory and infectious disease patterns are deeply interwoven with body composition and nutritional status (McDade, 2012;Urlacher et al, 2016Urlacher et al, , 2018 and, because of this small sample size, we cannot speak to their effects here.…”

“…After infection with STHs and other macro-parasites, IgE remains elevated for years, with high levels representing repeated infection over a long period of time (Iancovici et al, 2005;Urlacher et al, 2018). After infection with STHs and other macro-parasites, IgE remains elevated for years, with high levels representing repeated infection over a long period of time (Iancovici et al, 2005;Urlacher et al, 2018).…”

“…However, Shuar are currently experiencing increasingly rapid but widely variable market integration (i.e., the degree of production for and consumption from marketbased economies) within and across communities. Market integration among the Shuar has increased variation in several aspects of infrastructure and lifestyle, including in healthcare, house construction, sanitation, and exposure to pathogens (e.g., STHs; Cepon-Robins et al, 2014;Gildner et al, 2016;Liebert et al, 2013;Stagaman et al, 2018;Urlacher et al, 2016;Urlacher et al, 2018).…”

Epigenetic aging in children from a small‐scale farming society in The Congo Basin: Associations with child growth and family conflict

“…Specifically, they were likely better able to stave off infections, both relatively recently (WFH) and across the span of their growth during development (height‐for‐age) (Bogin & Varela‐Silva, ; Froment, ). When children are undernourished or face energetic stress due to infectious disease pressures, their bodies will necessarily downregulate growth in the face of limited resources (McDade et al, ; Urlacher et al, ). Our past correlative findings for Bondongo children's inflammatory and growth markers were consistent with this perspective (Boyette et al, ).…”