Context- and sex-dependent links between sire sexual success and offspring pathogen resistance

Abstract

Sexual selection has been proposed to promote genetic variants that improve resistance to pathogens (a special case of the "good genes" hypothesis). Yet, experimental tests of this hypothesis are scarce and equivocal. It is often assumed that additive genetic correlation between sexual traits and pathogen resistance is generated by their shared dependence on genetically variable "condition" of the organism. However, an alternative scenario posits condition-independent genetic variation in pathogen resistance; individuals more resistant to currently prevalent pathogens remain healthier and can invest more in sexual traits, but this advantage disappears in the absence of pathogens. Here, we tested whether Drosophila melanogaster males that are more sexually competitive (in terms of paternity share) sire offspring that are more resistant to the fungal pathogen Metarhizium brunneum. Furthermore, to investigate the importance of epidemiological context, we exposed sires to either an infection or a sham treatment before mating, to test whether the sire-offspring relationship depends on the presence of pathogens during sexual selection. We found that the relationship between sires sexual success and offspring pathogen resistance not only depended on sires exposure to the pathogen, but also on offspring sex. Sires that were more sexually successful in the absence of the pathogen had less resistant offspring whereas no relationship was detected for sires that competed for paternity after pathogen exposure. For daughters, the relationship tended to be negative irrespective of sire pathogen exposure. In no case was a positive correlation predicted by the "good genes" hypothesis detected. Thus, while sexual selection may act on genes affecting resistance in a context- and sex-dependent manner, we found no circumstances under which it promoted resistance.