Associations between male testosterone and immune function in a pathogenically stressed forager‐horticultural population

Abstract

Objectives Despite well-known fitness advantages to males who produce and maintain high endogenous testosterone levels, such phenotypes may be costly if testosterone-mediated investment in reproductive effort trade-off against investment in somatic maintenance. Previous studies of androgen-mediated trade-offs in human immune function find mixed results, in part because most studies either focus on a few indicators of immunity, are confounded by phenotypic correlation, or are observational. Here the association between male endogenous testosterone and 13 circulating cytokines are examined before and after ex vivo antigen stimulation with phytohaemagglutinin (PHA) and lipopolysaccharides (LPS) in a high pathogen population of Bolivian forager-horticulturalists. Materials and Methods A Milliplex 13-plex cytokine panel measured cytokine concentration in whole blood samples from 109 Tsimane men aged 40–89 (median=50 years) before and after antigen stimulation with PHA and LPS. Urinary testosterone was measured via enzyme immunoassay; demographic and anthropometric data were collected as part of the Tsimane Health and Life History Project. Results Higher endogenous testosterone was associated with down-regulated responses in all cytokines after PHA stimulation (but significantly in only 2/13 cytokines), controlling for age and body mass index. In contrast, testosterone was not significantly associated with down-regulation of cytokines after LPS stimulation. MANOVAs indicate that men with higher testosterone showed reduced cytokine responses to PHA compared to LPS (p=0.0098). Discussion Endogenous testosterone appears to be immunomodulatory rather than immunosuppressive. Potentially costlier forms of immune activation like those induced by PHA (largely T-cell biased immune activation) are down-regulated in men with higher testosterone, but testosterone has less impact on potentially less costly immune activation following LPS stimulation (largely B-cell mediated immunity).

Androgen Levels and Body Size Are Associated with Directional as Well as Fluctuating Asymmetry Patterns in Adult !Kung San and Kavango Males from Northern Namibia

“…Consequently it was assumed that a testosterone mediated suppressed immune function increases potential stress phases such as diseases or parasite load which may result in increased FA. Recent analyses among Tsimane foragers, however, revealed that endogenous testosterone appears to be immunomodulatory rather than immunosuppressive [93]. In the present study, adult androgen levels were weakly related to patterns of asymmetry.…”

Centennial perspective on human adaptability

“…Since the 1990s, researchers in human biology have become increasingly interested in better understanding the ecology and adaptive dimensions of immune function (McDade & Worthman, ; Shell‐Duncan, ; Ulijaszek, ). While the synergistic interaction between infections and nutrition has been long recognized (Hoffman‐Goetz, ; Scrimshaw, Taylor, & Gordon, ), only recently have scholars begun to examine human immune function and development from an evolutionary and life history perspective (McDade, ; McDade, Georgiev, & Kuzawa, ; Trumble et al, ). Such research recognizes the central role that immune function has in determining and regulating the allocation of energy at different stages of the life cycle.…”

Adiposity, CVD risk factors and testosterone

“…While T’s interfaces with the immune system have been extensively reviewed elsewhere, various lines of evidence suggest that elevated T tends to suppress or dampen certain immune functions, such as aspects of the inflammatory response, B-cell development and differentiation, and costly forms of T cell-mediated immune responses [2, 21, 25, 26]. Meanwhile, the body also down-regulates T production during acute infection, reflecting a fundamental life history trade-off that adaptively prioritizes energetic investment in survival over reproduction [26].…”