Ecological immunology in meerkats: testing environmental, social, hormonal, and transgenerational factors
Much of our knowledge of the mammalian immune system comes from laboratory studies of model organisms in highly controlled settings; however, in nature, organisms experience myriad biotic and abiotic pressures that can influence the immune response. Understanding how the immune system operates in natural systems therefore requires studies of animals living in socially and ecologically relevant environments. Here, I investigated the drivers of individual variation in immunocompetence in a wild population of meerkats (Suricata suricatta) living in the Kalahari Desert. The meerkat is characterised by aggressively mediated female social dominance, and although hormonal masculinization is present to varying degrees in all adult, female meerkats, the dominant female in each clan has greater concentrations of total androgens than does any other clan member. I therefore tested if the immunocompetence handicap hypothesis (ICHH), which posits that androgens in males mediate a trade off between reproductive success and immunocompetence, could apply to females and perhaps extend to their offspring. From 2012-2015, I followed and sampled approximately 300 meerkats living in 24 social clans. I related measures of immunocompetence (i.e., gastrointestinal parasite burdens and innate immune function) to environmental, demographic, social, and endocrine variables. I tested for transgenerational effects of maternally derived androgens on offspring immunocompetence by administering an antiandrogen to pregnant dominant dams. For adult meerkats, I found that there is a cost to dominance, in terms of reduced immunocompetence and that those with greater androgen concentrations (either inferred from fecal androgen metabolites or measured directly from blood as androstenedione, A4) had greater parasite burdens and weaker immune responses. Because, in female meerkats, A4 appears to exert the dual effects of promoting reproductive success and compromising immunity, I propose that the ICHH can apply to females. Moreover, the immunosuppressive consequences of female hormonal masculinization extend beyond the dams to their offspring, via prenatal exposure to raised androgens, and therefore may represent a transgenerational consequence of sexual selection operating in females. By studying immune function in natural systems, we can gain a broader perspective on immune function from an ecological and evolutionary context.
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