Parasite resistance has been proposed as an important driver of female choice for males with high quality, or ‘bright’ ornaments. As infection commonly affects the brightness of male ornaments, females may use these to discriminate between males based on their past or present infection load (Hamilton-Zuk hypothesis). However, the typically aggregated distribution of parasites among hosts, with a small proportion harbouring the majority of parasites, limits the generality of this hypothesis. The role of parasites in sexual selection would be more broadly applicable if male ornaments honestly indicate defence against parasites even in the absence of infection. Here, we tested whether the size, colour saturation, and left-right symmetry of a male guppy’s, Poecilia reticulata, ornaments before infection forecast his resistance to and tolerance of subsequent experimental infection with Gyrodactylus turnbulli. We found that some aspects of male ornaments are correlated with response to infection. This finding leads to the prediction that populations in which females show strong preferences for these male traits should have reduced transmission, potentially higher rates of resistance, and thus lower parasite prevalence. We used published data to test whether guppy populations in which female preference for the brightest males is strongest have the lowest parasite prevalence.
Results/Conclusions
In our experimental infection, males with more symmetrical melanin-based (black) colouration and those with larger areas of carotenoid (orange) colouration were more resistant. Additionally, males with more saturated orange colouration were less resistant to, but more tolerant of infection. Females choosing males with more symmetrical colouration, and larger orange ornaments, may therefore be less likely to contract an infection, and more likely to pass genetically determined parasite resistance to their offspring. A literature review yielded several populations for which we could match published female preference data and parasite prevalence data using GPS coordinates. Populations in which females have been shown to significantly prefer males with larger orange ornaments had significantly lower Gyrodactylus spp. prevalence than those in which females showed no significant preference for orange. Furthermore, among populations in which female preference had been assessed in the same paper and could therefore be directly compared, we found a significant negative correlation between the strength of the females’ preference for orange and Gyrodactylus spp. prevalence. These correlational results raise the intriguing possibility that female mate choice preferences may influence disease dynamics at the population scale. We discuss how these results offer new insight into the interaction between parasites and sexual selection.