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.