On sexual dimorphism in immune function

Abstract

Sexual dimorphism in immune function is a common pattern in vertebrates and also in a number of invertebrates. Most often, females are more 'immunocompetent' than males. The underlying causes are explained by either the role of immunosuppressive substances, such as testosterone, or by fundamental differences in male and female life histories. Here, we investigate some of the main predictions of the immunocompetence handicap hypothesis (ICHH) in a comparative framework using mammals. We focus specifically on the prediction that measures of sexual competition across species explain the observed patterns of variation in sex-specific immunocompetence within species. Our results are not consistent with the ICHH, but we do find that female mammals tend to have higher white blood cell counts (WBC), with some further associations between cell counts and longevity in females. We also document positive covariance between sexual dimorphism in immunity, as measured by a subset of WBC, and dimorphism in the duration of effective breeding. This is consistent with the application of 'Bateman's principle' to immunity, with females maximizing fitness by lengthening lifespan through greater investment in immune defences. Moreover, we present a meta-analysis of insect immunity, as the lack of testosterone in insects provides a means to investigate Bateman's principle for immunity independently of the ICHH. Here, we also find a systematic female bias in the expression of one of the two components of insect immune function that we investigated (phenoloxidase). From these analyses, we conclude that the mechanistic explanations of the ICHH lack empirical support. Instead, fitness-related differences between the sexes are potentially sufficient to explain many natural patterns in immunocompetence.

Figure 1

Juveniles (diamonds) have significantly more lymphocytes than adults (squares) in mammals. Whiskers indicate standard error.

Figure 2

There is no significant relationship between dimorphism in body mass and dimorphism in lymphocyte counts in mammals.

Figure 3

Sex differences in breeding duration and lymphocyte counts. Sex differences in DEB covary positively with sex differences in lymphocyte counts after controlling for body mass effects. The x-axis represents residuals from the regression of the DEB ratio on body mass.

Figure 4

(a) Effect size of male and female phenoloxidase activity as a function of sample size. The solid line indicates zero effect size, i.e. no sexual dimorphism in immune function. Data points above this line represent studies in which females were found to have higher phenoloxidase activity. The dashed line denotes the mean effect size, which was 0.187. (b) Effect of male and female haemocyte counts as a function of sample size. The solid and dashed lines represent zero and mean effect size, respectively. The mean effect size was 0.013. The data points above the zero line indicate higher female haemocyte counts; those below the line suggest higher counts in males. The mean effect size is slightly above the zero line, suggesting a very weak sexual dimorphism in haemocyte counts in the direction of higher values in females.