Experimentally altered male mating behaviour affects offspring exploratory behaviour via nongenetic paternal effects

Evidence is emerging that fathers can have nongenetic effects on the phenotypes of their offspring. Most studies have focused on the role that nongenetic modifications to sperm can have on offspring phenotype; however, fathers can also have nongenetic effects on offspring through their interactions with females, called female-mediated paternal effects. These effects can occur in situations where male phenotype, e.g. behaviour or morphology, affects female stress and/or provisioning of offspring. These effects are potentially widespread, but few studies have explicitly investigated the role of female-mediated paternal effects on offspring phenotype. Here, we asked if male mating interactions can affect offspring via female mediated paternal effects in the Trinidadian guppy, Poecilia reticulata. To do this, we manipulated mating behaviour by: (i) administering a drug known to affect the neurotransmitter dopamine, and (ii) varying the familiarity of potential mates, which affects attractiveness in this species. With these treatments, we successfully manipulated the mating behaviour of male guppies and female preference for those males. Further, we found significant effects of sire mating behaviour, sire drug treatment, and parental familiarity status on behavioural measures of offspring anxiety in response to a novel object. Because Control offspring of 'familiar' and 'unfamiliar' pairs differed in their behaviour, our results cannot be solely attributed to potential nongenetic modifications to sperm caused by the drug. These results emphasize the importance of female-mediated paternal effects, including those caused by altered male mating behaviour, in shaping offspring phenotype.