Sex-specific transgenerational plasticity in threespined sticklebacks

Sex-specific selection pressures can generate different phenotypic optima for males and females in response to the current environment, i.e. sex differences in phenotypic plasticity. Less widely appreciated is the possibility that transgenerational plasticity (TGP) can also depend on sex. Sex-specific TGP is potentially of great evolutionary significance, as it is a mechanism by which mothers and fathers can exert different effects on offspring traits and by which potentially adaptive traits can persist selectively across generations via only daughters or sons. Here, we demonstrate that maternally- and paternally-mediated TGP in response to predation risk have largely distinct effects on offspring traits in threespined sticklebacks (). Predator-exposed fathers produced sons that were more risk-prone, while predator-exposed mothers produced more anxious sons and daughters. Further, when combined together, maternal and paternal environments on offspring survival were nonadditive. Such sex-specific effects could occur if predation risk causes mothers and fathers to activate different developmental programs in sons versus daughters. Consistent with this hypothesis, offspring brain gene expression profile depended on whether their mother and/or father had been exposed to risk, and the influence of maternal and paternal environments varied between male and female offspring. Altogether these results draw attention to the potential for sex to influence patterns of TGP, and raise new questions about the evolution of plasticity at the interface between sexual conflict and parent-offspring conflict, with paternal strategies, maternal strategies, and offspring counter adaptations all ultimately dictating offspring phenotypes.