Experimental parasite infection reveals costs and benefits of paternal effects

Forces shaping an individual's phenotype are complex and include transgenerational effects. Despite low investment into reproduction, a father's environment and phenotype can shape its offspring's phenotype. Whether and when such paternal effects are adaptive, however, remains elusive. Using three-spined sticklebacks in controlled infection experiments, we show that sperm deficiencies in exposed males compared to their unexposed brothers functionally translated into reduced reproductive success in sperm competition trials. In non-competitive fertilisations, offspring of exposed males suffered significant costs of reduced hatching success and survival but they reached a higher body condition than their counterparts from unexposed fathers after experimental infection. Interestingly, those benefits of paternal infection did not result from increased resistance but from increased tolerance to the parasite. Altogether, these results demonstrate that parasite resistance and tolerance are shaped by processes involving both genetic and non-genetic inheritance and suggest a context-dependent adaptive value of paternal effects.