A female‐biased gene expression signature of dominance in cooperatively breeding meerkats

Author:

Campbell C. Ryan1ORCID,Manser Marta234,Shiratori Mari5ORCID,Williams Kelly1,Barreiro Luis5,Clutton‐Brock Tim346,Tung Jenny1789ORCID

Affiliation:

1. Department of Evolutionary Anthropology Duke University Durham North Carolina USA

2. Department of Evolutionary Biology and Environmental Studies University of Zurich Zurich Switzerland

3. Kalahari Research Centre, Kuruman River Reserve Northern Cape South Africa

4. Mammal Research Institute University of Pretoria Pretoria South Africa

5. Section of Genetic Medicine, Department of Medicine University of Chicago Chicago Illinois USA

6. Large Animal Research Group, Department of Zoology University of Cambridge Cambridge UK

7. Department of Biology Duke University Durham North Carolina USA

8. Duke Population Research Institute Duke University Durham North Carolina USA

9. Department of Primate Behavior and Evolution Max Planck Institute for Evolutionary Anthropology Leipzig Germany

Abstract

AbstractDominance is a primary determinant of social dynamics and resource access in social animals. Recent studies show that dominance is also reflected in the gene regulatory profiles of peripheral immune cells. However, the strength and direction of this relationship differs across the species and sex combinations investigated, potentially due to variation in the predictors and energetic consequences of dominance status. Here, we investigated the association between social status and gene expression in the blood of wild meerkats (Suricata suricatta; n = 113 individuals), including in response to lipopolysaccharide, Gardiquimod (an agonist of TLR7, which detects single‐stranded RNA in vivo) and glucocorticoid stimulation. Meerkats are cooperatively breeding social carnivores in which breeding females physically outcompete other females to suppress reproduction, resulting in high reproductive skew. They therefore present an opportunity to disentangle the effects of social dominance from those of sex per se. We identify a sex‐specific signature of dominance, including 1045 differentially expressed genes in females but none in males. Dominant females exhibit elevated activity in innate immune pathways and a larger fold‐change response to LPS challenge. Based on these results and a preliminary comparison to other mammals, we speculate that the gene regulatory signature of social status in the immune system depends on the determinants and energetic costs of social dominance, such that it is most pronounced in hierarchies where physical competition is important and reproductive skew is large. Such a pattern has the potential to mediate life history trade‐offs between investment in reproduction versus somatic maintenance.

Funder

North Carolina Biotechnology Center

Division of Integrative Organismal Systems

Human Frontier Science Program

H2020 European Research Council

National Institute on Aging

Publisher

Wiley

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