DOI: 10.1093/emph/eoag013 ISSN: 2050-6201

Amazonian Shuar testosterone levels are related to parasite infection: Immunocompetence Handicap Hypothesis Implications

Theresa E Gildner, Aaron D Blackwell, Melissa A Liebert, Samuel S Urlacher, Tara J Cepon-Robins, Joshua M Schrock, Richard G Bribiescas, Felicia C Madimenos, J Josh Snodgrass, Lawrence S Sugiyama

Abstract

Background and objectives

Testosterone is hypothesized to influence energetic tradeoffs between male reproduction and immune function. Testosterone is generally thought to be immunosuppressive, with high testosterone levels signaling male health and infection resistance. The Immunocompetence Handicap Hypothesis (ICHH) posits that testosterone’s role in developing male secondary sexual characteristics and suppressing immune function creates a tradeoff between testosterone-linked traits and immunocompetence. Yet, the immune effects of testosterone in humans remain poorly understood. Research is particularly limited among energetically constrained, natural fertility populations characterized by high pathogen loads and long-lasting infections (such as parasitic disease), characteristics relevant to the evolution of hypothesized testosterone-linked tradeoffs.

Methodology

We test whether salivary testosterone concentrations are associated with parasitic helminth infection status and parasite load among 90 Indigenous Shuar males aged 12–67 years.

Results

Higher testosterone levels were associated with increased infection risk but lower parasite load. However, these findings were only evident among adolescents (ages 12–19) and only for Trichuris trichiura (whipworm) but not Ascaris lumbricoides (roundworm) infections.

Conclusions and implications

These findings suggest higher testosterone may increase the risk of becoming infected with some parasite species, but that heavy pathogen loads lead to a shift in resource allocation from testosterone production to immune activity during a life stage with high testosterone-related energetic demands. While some results aligned with the ICHH, the significant effects of participant age and parasite species on testosterone-infection associations indicate that the ICHH does not completely capture the full complexity of human immune-related life history tradeoffs and variation in host–parasite interactions.

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