Indirect Benefits Due to Genes for Parasite Tolerance
Females may also choose mates based on their ability to tolerate parasites. Hosts may diminish the negative impacts of parasites through resistance or tolerance: Resistance includes behaviours and physiological responses that allow individuals to avoid becoming infected, while tolerance involves diminishing the negative effects of infection once infected (Råberg et al. 2007; Best et al.2008; Råberg et al. 2009). Theoretical models of sexual selection and female choice often posit that extravagant male traits are an indicator of a male’s underlying ability to resist infection, and so females choose flashy males in order to gain indirect benefits of increased resistance in their offspring (Hamilton & Zuk 1982; Andersson 1994). However, becoming infected involves an element of chance, whereas being able to tolerate infection is only possible if that animal truly has a physiology capable of such tolerance. There could, therefore, be a selective advantage for females to attend to a male’s quality and vigor despite his infection, which would set the stage for the evolution of mimicry.
There is some circumstantial evidence rendering it plausible that females could prefer infected mates due to their ability to tolerate infection. The ability of individuals to tolerate infection has been shown to vary in wild populations of dace, and this variability seems to be genetically mediated (Blanchet et al. 2010), potentially allowing inherited offspring tolerance to be an indirect benefit to females. In these dace, and in mice, parasite resistance and tolerance are negatively correlated, suggesting a trade-off between investment in each mechanism (Råberg et al. 2007; Blanchet et al. 2010). Female white-footed mice prefer to mate with males who are infested with bot fly larvae, possibly because their ability to continue functioning in the face of infection indicates tolerance to females (Cramer & Cameron 2007). Thus, under certain circumstances, it is possible that females might select males as fathers who will provide indirect genetic benefits in terms of parasite tolerance rather than resistance.
Tolerance is usually measured as the steepness of the slope of a regression of host fitness against infection burden (Simms & Triplett 1994; Koskela et al. 2002). As such, females could use the mismatch between a male’s level of parasitic infection and his performance of other fitness-enhancing behaviours to evaluate tolerance. For instance, a male who can perform an energetically vigorous display while being heavily parasitized could be selected by females (i.e., a parasite-mediated handicap). By this same logic, a male who artificially augments his apparent parasite burden and so appears to be more heavily infected than he really is, could make any energetic display he does seem more impressive. A parasite that is highly costly to males would allow a mismatch between infection status and vigour to be particularly informative to females, while also effectively deterring rivals.
How prevalent a parasite is in a population is likely to influence the benefits of female choice for tolerance and resistance. In the white-footed mouse example mentioned above, the authors proposed that tolerance may be highly beneficial due to the ubiquitous nature of bot fly infections, which infect 69.8% of males (Cramer & Cameron 2006, 2007). It is likely that, the more ubiquitous a parasite is in a population, the stronger will be the selection pressures on females to ensure their offspring inherit genes promoting tolerance. This is because the chances of offspring experiencing infection are high. In populations in which a certain infection is ubiquitous, it is unlikely that many mimics will avoid becoming truly infected. However, depending on how females evaluate potential mates, if a male were to exaggerate or augment his apparent parasite-load, he could still increase the above-mentioned mismatch between his vigour and apparent parasite burden. Thus, if females evaluate male vigour and apparent parasite load on a continuous scale (see: Kennedy et al. 1987; Zuk 1988; Buchholz 1995), rather than classifying males dichotomously as either infected or not, mimic signals which exaggerate infection could still make males appear more parasite-tolerant. As such, parasite prevalence and female evaluation heuristics will shape the likelihood that mimicry will evolve.