Paternal care effects outweigh gamete-mediated and personal environment effects during the transgenerational estimation of risk in fathead minnows

BACKGROUND: Individuals can estimate risk by integrating prenatal with postnatal and personal information, but the relative importance of different information sources during the transgenerational response is unclear. The estimated level of risk can be tested using the cognitive rule of risk allocation, which postulates that under consistent high-risk, antipredator efforts should decrease so that individual metabolic requirements can be satisfied. Here we conduct a comprehensive study on transgenerational risk transmission by testing whether risk allocation occurs across 12 treatments that consist of different maternal, paternal, parental care (including cross-fostering) and offspring risk environment combinations in the fathead minnow Pimephales promelas, a small cyprinid fish with alloparental care. In each risk environment, we manipulated perceived risk by continuously exposing individuals from birth onwards to conspecific alarm cues or a control water treatment. Using 2810 1-month old individuals, we then estimated shoaling behaviour prior to and subsequent to a novel mechanical predator disturbance. RESULTS: Overall, shoals estimating risk to be high were denser during the prestimulus period, and, following the risk allocation hypothesis, resumed normal shoaling densities faster following the disturbance. Treatments involving parental care consistently induced densest shoals and greatest levels of risk allocation. Although prenatal risk environments did not relate to paternal care intensity, greater care intensity induced more risk allocation when parents provided care for their own offspring as opposed to those that cross-fostered fry. In the absence of care, parental effects on shoaling density were relatively weak and personal environments modulated risk allocation only when parental risk was low. CONCLUSIONS: Our study highlights the high relative importance of parental care as opposed to other information sources, and its function as a mechanism underlying transgenerational risk transmission. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12862-021-01919-1.