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

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 sires 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. Lay SummarySexual selection has been debated in relation to natural selection for decades. The "good genes" hypothesis which posits a positive genetic correlation between sexual success and non-sexual fitness, is often considered as a mechanism aligning sexual selection and natural selection. Scientists have long wondered if genetic variants that make individuals more sexually successful also enhance their ability to fight against pathogens, testing a special version of "good genes". However, evidence is mixed. Two key mechanisms linking sexual success and pathogen resistance have been proposed: the "condition- dependent" scenario, where general health improve both sexual traits and pathogen resistance, and the "context-dependent" scenario, where resistance to specific pathogens benefits sexual success only in certain environments. Few studies distinguish between these two mechanisms. This study examines both scenarios in Drosophila melanogaster, finding that the relationship between a sires mating success and offspring pathogen resistance to the fungal pathogen Metarhizium brunneum depends on sires pathogen exposure prior to measurement of sexual success and offspring sex. These findings challenge the "good genes" hypothesis and emphasize the necessity of including context in sexual selection studies.