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Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons.

Publication ,  Journal Article
Lea, AJ; Akinyi, MY; Nyakundi, R; Mareri, P; Nyundo, F; Kariuki, T; Alberts, SC; Archie, EA; Tung, J
Published in: Proceedings of the National Academy of Sciences of the United States of America
December 2018

In humans and other hierarchical species, social status is tightly linked to variation in health and fitness-related traits. Experimental manipulations of social status in female rhesus macaques suggest that this relationship is partially explained by status effects on immune gene regulation. However, social hierarchies are established and maintained in different ways across species: While some are based on kin-directed nepotism, others emerge from direct physical competition. We investigated how this variation influences the relationship between social status and immune gene regulation in wild baboons, where hierarchies in males are based on fighting ability but female hierarchies are nepotistic. We measured rank-related variation in gene expression levels in adult baboons of both sexes at baseline and in response to ex vivo stimulation with the bacterial endotoxin lipopolysaccharide (LPS). We identified >2,000 rank-associated genes in males, an order of magnitude more than in females. In males, high status predicted increased expression of genes involved in innate immunity and preferential activation of the NF-κB-mediated proinflammatory pathway, a pattern previously associated with low status in female rhesus macaques. Using Mendelian randomization, we reconcile these observations by demonstrating that high status-associated gene expression patterns are precursors, not consequences, of high social status in males, in support of the idea that physiological condition determines who attains high rank. Together, our work provides a test of the relationship between social status and immune gene regulation in wild primates. It also emphasizes the importance of social context in shaping the relationship between social status and immune function.

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Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

December 2018

Volume

115

Issue

52

Start / End Page

E12163 / E12171

Related Subject Headings

  • Social Dominance
  • Social Behavior
  • Sex Factors
  • Papio
  • Mendelian Randomization Analysis
  • Male
  • Macaca mulatta
  • Immunity, Innate
  • Hierarchy, Social
  • Gene Expression
 

Citation

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Lea, A. J., Akinyi, M. Y., Nyakundi, R., Mareri, P., Nyundo, F., Kariuki, T., … Tung, J. (2018). Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons. Proceedings of the National Academy of Sciences of the United States of America, 115(52), E12163–E12171. https://doi.org/10.1073/pnas.1811967115
Lea, Amanda J., Mercy Y. Akinyi, Ruth Nyakundi, Peter Mareri, Fred Nyundo, Thomas Kariuki, Susan C. Alberts, Elizabeth A. Archie, and Jenny Tung. “Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons.Proceedings of the National Academy of Sciences of the United States of America 115, no. 52 (December 2018): E12163–71. https://doi.org/10.1073/pnas.1811967115.
Lea AJ, Akinyi MY, Nyakundi R, Mareri P, Nyundo F, Kariuki T, et al. Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons. Proceedings of the National Academy of Sciences of the United States of America. 2018 Dec;115(52):E12163–71.
Lea, Amanda J., et al. “Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons.Proceedings of the National Academy of Sciences of the United States of America, vol. 115, no. 52, Dec. 2018, pp. E12163–71. Epmc, doi:10.1073/pnas.1811967115.
Lea AJ, Akinyi MY, Nyakundi R, Mareri P, Nyundo F, Kariuki T, Alberts SC, Archie EA, Tung J. Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons. Proceedings of the National Academy of Sciences of the United States of America. 2018 Dec;115(52):E12163–E12171.
Journal cover image

Published In

Proceedings of the National Academy of Sciences of the United States of America

DOI

EISSN

1091-6490

ISSN

0027-8424

Publication Date

December 2018

Volume

115

Issue

52

Start / End Page

E12163 / E12171

Related Subject Headings

  • Social Dominance
  • Social Behavior
  • Sex Factors
  • Papio
  • Mendelian Randomization Analysis
  • Male
  • Macaca mulatta
  • Immunity, Innate
  • Hierarchy, Social
  • Gene Expression