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

Abstract

Social status can mediate effects on the immune system, with profound consequences for individual health; nevertheless, most investigators of status-related disparities in free-ranging 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 female-dominant 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.

Sex and hatching order modulate the association between MHC‐II diversity and fitness in early‐life stages of a wild seabird

“…In addition, in kittiwakes, second-hatched chicks hatch from eggs containing increased levels of androgens compared to first-hatched chicks (Benowitz-Fredericks, Kitaysky, Welcker, & Hatch, 2013;Gasparini et al, 2007). This may lead to reduced immune responses as these sex hormones are known to be immunosuppressive in other species (Klein & Flanagan, 2016;Smyth, Caruso, Davies, Clutton-Brock, & Drea, 2018). Thus, females and second-hatched chicks are predicted to be immunologically disadvantaged compared to males and first-hatched chicks.…”

Deferred benefits of dominance for natal males in a cooperative breeder, the Kalahari meerkat

“…The exact costs of holding dominance for male meerkats are relatively unknown compared with females (e.g. Carlson et al, 2004;Hodge et al, 2008;Smyth et al, 2018) but may be lower: unlike in females, dominant male meerkats do not differ in testosterone or cortisol levels from their same-sex subordinates (Carlson et al, 2004;Davies et al, 2017). While some costs are likely to remainsuch as investment in dominance-maintaining behaviours like substrate marking and aggression towards same-sex subordinatesothers may be reduced for natal dominant males.…”

“…Kalahari meerkats are a classic cooperative breeding system, with substantial reproductive gains of taking dominance in both sexes (Hauber & Lacey, 2005;Spong et al, 2008) and correspondingly fierce competition for the position, often incurring high costs (see Carlson et al, 2004;Hodge et al, 2008;Smyth et al, 2018). Typically, a dominant female is natal to the group, while male dominants are unrelated immigrants (joining groups either singly or as part of a coalition) who may take dominance following the death/disappearance of the previous dominant male or may actively displace an incumbent (Clutton-Brock & Manser, 2016).…”

A heritable androgenic mechanism of female intrasexual competition in cooperatively breeding meerkats

“…Evidently protected from potential costs of early masculinisation (e.g. 20 ), meerkats, like other vertebrate females ( 48, 49 ), nonetheless experience costs of natural androgens (again, potentially differentiating androstenedione from testosterone), including increased parasitism ( 50 ) and reduced immunocompetence ( 51 ). Although androgen-mediated health costs may carry reproductive tradeoffs during environmental stressors ( 21 ), the socio-reproductive advantages appear to far outweigh these costs.…”

“…One treated female (9%) aborted and was excluded from the study; by comparison, 21% of the contemporaneous dominant controls aborted ( 21 ). Given the health costs of natural androgens to dominant female meerkats ( 50, 51 ), flutamide-treated dams were potentially less at risk than their control counterparts. A few subjects received antibiotic ointment to treat minor infections at the suture site, but these infections typically occurred after parturition (i.e., after the cessation of focal observations) and had no noticeable effects on behaviour.…”