Social and endocrine correlates of immune function in meerkats : implications for the immunocompetence

Abstract

Social status can mediate effects on the immune system, with profound consequences for individual health; nevertheless, most investigators of status-related disparities in freeranging animals have used faecal parasite burdens to proxy immune function in the males of male-dominant species. We instead use direct measures of innate immune function (complement and natural antibodies) to examine status-related immunocompetence in both sexes of a femaledominant species. The meerkat is a unique model for such a study because it is a cooperatively breeding species in which status-related differences are extreme, evident in reproductive skew, morphology, behaviour, communication and physiology, including that dominant females naturally express the greatest total androgen (androstenedione plus testosterone) concentrations. We found that, relative to subordinates, dominant animals had reduced serum bacteria-killing abilities; also, relative to subordinate females, dominant females had reduced haemolytic complement activities. Irrespective of an individual’s sex or social status, androstenedione concentrations (but not body condition, age or reproductive activity) negatively predicted concurrent immunocompetence. Thus, dominant meerkats of both sexes are immunocompromised. Moreover, in female meerkats, androstenedione perhaps acting directly or via local conversion, may exert a double-edged effect of promoting dominance and reproductive success at the cost of increased parasitism and reduced immune function. Given the prominent signalling of dominance in female meerkats, these findings may relate to the immunocompetence handicap hypothesis (ICHH); however, our data would suggest that the endocrine mechanism underlying the ICHH need not be mediated solely by testosterone and might explain trade-offs in females, as well as in males.This work was supported by the National Science Foundation (IOS-1021633 to C.M.D. and IOS-1601685 to C.M.D. and K.N.S.) and the Duke University Graduate School (Judy C. Woodruff Fellowship, Fred and Barbara Sutherland Fellowship and Katherine Goodman Stern Fellowship to K.N.S.). Vehicle costs in the field were supported by Duke University (research funds to C.M.D.). We relied on records of individual life histories and access to a field site maintained by the KalahariMeerkat Project (KMP). During the span of this study, the KMP was supported by the European Research Council (Research grant no. 294494 to T.H.C.-B.), the University of Cambridge, the University of Zurich, the Mammal Research Institute at the University of Pretoria and Duke University.http://rsos.royalsocietypublishing.orgam2019Mammal Research Institut

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