Bateman's principle and immunity

Abstract

The immunocompetence handicap hypothesis (ICHH) of Folstad and Karter has inspired a large number of studies that have tried to understand the causal basis of parasite-mediated sexual selection. Even though this hypothesis is based on the double function of testosterone, a hormone restricted to vertebrates, studies of invertebrates have tended to provide central support for specific predictions of the ICHH. I propose an alternative hypothesis that explains many of the findings without relying on testosterone or other biochemical feedback loops. This alternative is based on Bateman's principle, that males gain fitness by increasing their mating success whilst females increase fitness through longevity because their reproductive effort is much higher. Consequently, I predict that females should invest more in immunity than males. The extent of this dimorphism is determined by the mating system and the genetic correlation between males and females in immune traits. In support of my arguments, I mainly use studies on insects that share innate immunity with vertebrates and have the advantage that they are easier to study.

Examination of the immune responses of males and workers of the leaf-cutting ant Acromyrmex echinatior and the effect of infection

“…The reduced encapsulation response of workers 96 h after infection could therefore be due to depletion or to toxin-mediated immunodepression and further work is needed to distinguish these possibilities. The immune response is a costly trait (Kraaijeveld and Godfray, 1997;Fellowes et al, 1998;Kraaijeveld et al, 2002;Rolff, 2002;Rolff and Siva-Jothy, 2003;Schmid-Hempel, 2003;2005;Boomsma et al, 2005) and it is therefore to be expected that there are trade-offs involved in the allocation of resources to it. Investment will depend upon life-history and the importance of being resistant to diseases, while the response itself will be finite and may be depleted by multiple challenges.…”

“…Males have similarly been found to have lower immunocompetence than females in both of the other social insect species previously examined (Gerloff et al, 2003;Vainio et al, 2004; B. Baer and P. Schmid-Hempel, unpubl. ), as well as in some other insects (Adamo et al, 2001;Rolff, 2001Rolff, , 2002Siva-Jothy et al, 2001;SchmidHempel, 2005). Although the data in our study do not allow us to directly distinguish between haploid susceptibility and life-history as explanations for low male immunocompetence, there are two points that may shed light on the issue.…”

“…Workers are likely to be selected to be resistant to parasites both to maximise their individual value to their colony and to reduce the risk of them transmitting diseases to nestmates. The immune system of insects is costly (Kraaijeveld and Godfray, 1997;Fellowes et al, 1998;Kraaijeveld et al, 2002;Rolff and Siva-Jothy, 2003;SchmidHempel, 2003;2005), and the much lower importance of diseases to males compared to workers means that males may benefit by diverting resources from immunity to matingrelated traits (Rolff, 2002;Schmid-Hempel, 2005).…”

“…Consequently, social insects have evolved a number of specialised mechanisms to defend their colonies against parasites, including grooming, antibiotic secretions and hygienic behaviour (e.g. Kermarrec et al, 1986;Rosengaus et al, 1998Rosengaus et al, , 2000Rosengaus et al, , 2004Schmid-Hempel, 1998;Christie et al, 2002;Hart and Ratnieks, 2001;2002;Hughes et al, 2002;Poulsen et al, 2002a,b;Turillazzi et al, 2004;Boomsma et al, in press). The effectiveness of these mechanisms is such that rather than the group-living lifestyle being associated with increased susceptibility to disease, as is expected, it may instead result in decreased susceptibility (Rosengaus et al, 1998;Hughes et al, 2002;Shimizu and Yamaji, 2003).…”

Subtle effect of Xenos vesparum (Xenidae, Strepsiptera) on the reproductive apparatus of its male host: Parasite or parasitoid?

“…Females, instead, generally do not show this trade-off as they gain reproductive fitness by living longer (i.e. producing multiple offsprings), hence they evolved adaptations to maintain their immune competence at higher levels (Rolff, 2002). In social Hymenoptera it has also been proposed that males should be more sensitive to diseases because of their haploid condition that reduces the availability of genetic combinations capable to provide resistance against parasites (O'Donnell and Beshers, 2004).…”