Sex-specific transgenerational plasticity I: Maternal and paternal effects on sons and daughters

Transgenerational plasticity (TGP) or parental effects - when parental environments alter the phenotype of future generations - can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex - of both the parent and the offspring - plays an important role in driving the evolution of transgenerational plasticity in both adaptive and nonadaptive ways. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of threespined sticklebacks (Gasterosteus aculeatus) by independently and jointly manipulating maternal and paternal experiences and separately evaluating their phenotypic effects in sons versus daughters. We tested the adaptive hypothesis that daughters are more responsive to cues from their mother, while sons are more responsive to cues from their father. We exposed mothers, fathers, or both parents to visual cues of predation risk and measured offspring antipredator traits and brain gene expression. Predator-exposed fathers produced sons that were more risk-prone, while predator-exposed mothers produced more anxious sons and daughters. Further, maternal and paternal effects on offspring survival were nonadditive: offspring with a predator-exposed father, but not two predator-exposed parents, had lower survival against live predators. There were also strong sex-specific effects on brain gene expression: exposing mothers versus fathers to predation risk activated different transcriptional profiles in their offspring, and sons and daughters strongly differed in the ways in which their brain gene expression profiles were influenced by parental experience. We found little evidence to support the hypothesis that offspring prioritize their same-sex parent9s experience. Parental effects varied with both the sex of the parent and the offspring in complicated and nonadditive ways. Failing to account for these sex-specific patterns (e.g., by pooling sons and daughters) would have underestimated the magnitude of parental effects. Altogether, these results draw attention to the potential for sex to influence patterns of TGP and raise new questions about the interface between transgenerational plasticity and sex-specific selective pressures, sexual conflict, and sexual selection.