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

Benjamin Trumble, Aaron D. Blackwell, Jonathan Stieglitz, Melissa Emery Thompson, Ivan Maldonado Suarez, Hillard Kaplan, Michael Gurven

Research output: Contribution to journalArticle

12 Citations (Scopus)

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 phytohemagglutinin (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 with 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).

Original languageEnglish (US)
Pages (from-to)494-505
Number of pages12
JournalAmerican Journal of Physical Anthropology
Volume161
Issue number3
DOIs
StatePublished - Nov 1 2016

Fingerprint

activation
Testosterone
immunity
Phytohemagglutinins
Cytokines
Population
Lipopolysaccharides
fitness
regulation
health
Antigens
Immunosuppressive Agents
Immunoenzyme Techniques
Cellular Immunity
Androgens
Immunity
Body Mass Index
B-Lymphocytes
Down-Regulation
Maintenance

Keywords

  • immunocompetence handicap hypothesis
  • lipopolysaccharides (LPS)
  • phytohemagglutinin (PHA)
  • testosterone
  • Tsimane

ASJC Scopus subject areas

  • Anatomy
  • Anthropology

Cite this

Associations between male testosterone and immune function in a pathogenically stressed forager-horticultural population. / Trumble, Benjamin; Blackwell, Aaron D.; Stieglitz, Jonathan; Thompson, Melissa Emery; Suarez, Ivan Maldonado; Kaplan, Hillard; Gurven, Michael.

In: American Journal of Physical Anthropology, Vol. 161, No. 3, 01.11.2016, p. 494-505.

Research output: Contribution to journalArticle

Trumble, Benjamin ; Blackwell, Aaron D. ; Stieglitz, Jonathan ; Thompson, Melissa Emery ; Suarez, Ivan Maldonado ; Kaplan, Hillard ; Gurven, Michael. / Associations between male testosterone and immune function in a pathogenically stressed forager-horticultural population. In: American Journal of Physical Anthropology. 2016 ; Vol. 161, No. 3. pp. 494-505.
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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 phytohemagglutinin (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 with 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).",
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