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

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.

Testosterone, body size, and sexual signals predict parasite load in Yarrow’s Spiny Lizards (Sceloporus jarrovii)

Parasite load significantly impacts host health and fitness and may vary substantially among individuals within a population. The immunocompetence handicap hypothesis posits that sexual signals are honest indicators of male quality because they are maintained by testosterone, an immunosuppressant that yields higher parasite loads. Additionally, testosterone may influence parasite load by increasing activity levels. We examined these two hypotheses in a wild population of Yarrow’s Spiny Lizards (Sceloporus jarrovii Cope, 1875) in Arizona. We (i) compared fecal testosterone levels to ectoparasite and haemoparasite loads, (ii) tested if sexual signals (total coloured area, aggression, and head size), locomotor activity, and body size correlated with testosterone levels, and (iii) compared sexual signals, locomotor activity, and body size to parasite load. Ectoparasite loads increased with total coloured area and tended to increase with testosterone, but this latter relationship was only nearly significant. Parasite loads increased with body size. Thus, we found some support for the immunocompetence handicap hypothesis and none for the activity hypothesis. Our results are consistent with an alternative hypothesis that larger individuals have more parasites because they have more surface area and (or) have had longer to accumulate parasites. Future studies should examine the relative contributions of testosterone and glucocorticoids in driving variation in parasite loads.

Test of immunocompetence handicap hypothesis in mice (Mus musculus) infected with Trichinella spiralis

The immunocompetence handicap hypothesis (ICHH) proposes that testosterone enhances the expression of sexual traits but suppresses immune function. However, studies to test the hypothesis have shown mixed results. Alternatively, sexual traits, immune function, and parasite susceptibility may be mediated by the stress hormone corticosterone. Here, we report an experimental test of the ICHH that included the manipulation of both testosterone and parasites in male laboratory mice (Mus musculus L., 1758). We conducted a factorial experiment, injecting each individual mouse with testosterone or not and infecting them with the nematode parasite Trichinella spiralis (Owen, 1835) or not. As predicted, testosterone enhanced the scent attractiveness of male mice, whereas parasite infection reduced it, but only in male mice not injected with testosterone. However, we found no evidence that corticosterone is involved in mediating the effects of testosterone. These results confirm that maintaining high testosterone levels entails the cost of increased parasite abundance. This study provides direct evidence supporting the ICHH.

Secondary sexual coloration is related to white blood cell counts and testosterone in male southeastern five-lined skinks (Plestiodon inexpectatus)

The immunocompetence handicap hypothesis posits that secondary sexual coloration can honestly signal male quality because elevated testosterone, which is necessary for the expression of the coloration, also handicaps males through immunosuppression. Thus only high quality males can express the showiest coloration in spite of immunosuppression. Here we report a test of the immunocompetence handicap hypothesis in southeastern five-lined skinks, Plestiodon inexpectatus, which exhibit a reddish-orange head coloration during the breeding season. We tested whether head coloration is related to circulating testosterone concentrations and reflects the status of a male’s immune system, as measured by total leukocyte counts. As predicted, hue, saturation, and extent of head coloration were correlated with plasma testosterone, and the brightness of the head was negatively correlated with total circulating leukocytes. While results are consistent with the immunocompetence handicap hypothesis, additional studies that include experimental manipulations of testosterone levels and measure other aspects of immunity are warranted.