Sexbiased parasitism

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Male and female life histories are usually very different, especially in species with highly polygynous mating systems, in which females maximize fitness by living for a long time and producing many young, and males maximize fitness by mating with many reproductively active females (Bateman, 1948; Trivers, 1972). These disparate selection pressures often lead to the production of weapons and ornaments in males, as well as large body size, especially in mammals (Andersson, 1994). These traits are envisaged to be costly to produce and maintain and, in mammals, it has been shown that in species in which there is strong sexual selection (as measured by mating system and sexual size dimorphism), males appear to suffer viability costs (i.e. there is male-biased mortality). Recently, it has been suggested that one mechanism by which this viability cost might be exerted is via increased susceptibility or exposure to parasites (Moore and Wilson, 2002). Indeed, across a range of mammal species, males suffer significantly greater prevalence of parasitism (via a range of parasites and pathogens) than do females, and this sex-bias in parasitism (SBP) is positively correlated with the strength of sexual selection: SBP is greater in polygynous than monogamous species, and is positively correlated with the extent of sexual size dimorphism (Moore and Wilson, 2002), but not with sex differences in home-range size (Wilson et al., 2003b). Moreover, there was a positive correlation between SBP and sex-biased mortality, with species in which there was male-biased parasitism also exhibiting male-biased mortality. These analyses are consistent with the idea that sexual selection imposes a viability cost on males and that this cost is mediated, in part at least, by sex differences in parasitism, although the precise mechanism causing differential parasitism of the sexes remains to be identified (Moore and Wilson, 2002).

If sex-biased parasitism is a general cost of sexual selection, then we should also observe SBP in other taxonomic groups. Sex differences in parasitism have been observed in humans (e.g. Owens, 2002; Wilson et al., 2003b) and birds (Poulin, 1996), but were not found in fish (Poulin, 1996) or in invertebrates, including insects (Sheridan et al., 2000). However, a recent study of insects, using a much larger dataset than that used by Sheridan and colleagues, observed a small, but highly significant, male-bias in the prevalence of parasitism by a range of entomopathogens (S.L. Moore and K. Wilson, unpublished). Moreover, as with the mammal analysis, the male bias was statistically significant for polygynous species, but not for non-polygynous (monogamous and polyandrous) ones, and was significantly positively correlated with the degree of sexual size dimorphism.

Interestingly, a meta-analysis of published information on sex differences in traits associated with immune function in insects, namely haemocyte number, antibacterial activity and phenoloxidase activity, indicated that females have consistently higher levels than males (S.L. Moore and K. Wilson, unpublished). Thus, sex differences in immune function may explain why males are generally more heavily parasitized than females, though clearly more detailed species-specific studies are required. This result is particularly interesting because it shows that in both vertebrates and invertebrates females have better immunity and lower parasite loads than males, suggesting a common explanation. This is interesting because it suggests that we can probably dismiss the immuno-depressive effects of testosterone as an important explanation for sex differences in parasitism in vertebrates (Folstad and Karter, 1992), since we get the same pattern in insects which, of course, lack testosterone or any sex-specific hormones (Nijhout, 1994). However, recent studies have shown that mating may have immunodepressive side effects in insects (e.g. McKean and Nunney, 2001; Rolff and Siva-Jothy, 2002), and that these effects may be mediated by juvenile hormone (Rolff and Siva-Jothy, 2002). So, if some males mate more frequently, on average, than females, then they may spend relatively more time in an immunodepressed state and this might explain their greater parasitism.

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