A female-biased gene expression signature of dominance in cooperatively breeding meerkats
Dominance is a primary determinant of social dynamics and resource access in social animals. Recent studies show that differences in dominance are 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 so far, potentially due to variation in the predictors and energetic consequences of dominant status. To test this possibility, we investigated the association between social status and gene expression in the blood of wild meerkats in the Kalahari Desert of South Africa, including in response to lipopolysaccharide, Gardiquimod, and glucocorticoid stimulation (n=740 samples; 113 meerkats). Meerkats are cooperatively breeding social carnivores in which breeding females physically outcompete other females and reproductive skew is high. 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 1,045 differentially expressed genes in females but none in males. Dominant females exhibit elevated activity in innate immune pathways, as well as an exacerbated immune response to LPS challenge. Female meerkats therefore resemble male baboons, where physical competition is also central to determining rank hierarchies and mating effort is high, but differ from female primates in which social status is determined by nepotism. Our results support the hypothesis that the gene regulatory signature of social status depends on the determinants and energetic costs of social dominance. They also support potential life history trade-offs between investment in reproduction versus somatic maintenance. Overall design: We purified PBMCs from ~1 mL of blood per blood draw via density gradient centrifugation, typically within 3 – 4 hours of the original blood draw. For each blood sample, we plated 200,000 PBMCs in 200 µL cell suspension into each of four tissue culture wells containing 20 µL cell culture media (RPMI; 10% FBS; 1% penicillin-streptomycin), for a total volume of 220 µL. Purified PBMCs from each sample were cultured for 4 hours in (i) media only (control condition), (ii) media with 10 ng/mL lipopolysaccharide (LPS from the E. coli O111:B4 strain), to mimic bacterial exposure; (iii) media plus 1.0 µg/mL Gardiquimod (Gard), which activates Toll-like receptor 7 signaling; or (iv) media plus 1.0 µM Dexamethasone (Dex), a synthetic glucocorticoid. The cells were then incubated in parallel for 4 hours (37 C and 5% CO2), washed with 1× PBS, lysed, and stored immediately at -80° C until library preparation.