Transgenerational plasticity of exploratory behavior and a hidden cost of mismatched risk environments between parental sexes

We require a better understanding of the relative contribution of different modes of non-genetic inheritance in behavioral trait development. Thus, we investigate variation in exploratory behavior, which is ecologically relevant and a target of selection. The metabolic hypothesis predicts exploratory behavior to be size-dependent across taxa. This size-dependency is cancelled out under high perceived risk, allowing us to determine the transgenerationally integrated estimated level of risk. Using fathead minnows Pimephales promelas, we manipulated perceived risk in mothers, fathers, caring males and offspring through continuous exposure to either conspecific alarm cues or to a control water treatment. In 1000 four-month old offspring, we determined body sizes and exploratory behavior. Perceived high risk in mothers, followed by personal risk, was most effective in eliminating size-dependent behavior whereas effects of paternal risk on offspring behavioral development were substantially weaker. When maternal risk is high, environmental mismatches between parents prevented offspring from responding appropriately to personal high risk. The environment of the caring male also impacted offspring behavior to a greater extent than that of its genetic parents. Our study highlights the high relative importance of maternal, personal and caring male risk environments and showcases potential costs of an environmental mismatch between parental sexes.