Vertical transmission of horizontally acquired social information in sticklebacks: Implications for transgenerational plasticity

There is growing evidence that offspring receive information about their environment vertically, i.e. from their parents (environmental parental effects or transgenerational plasticity). For example, parents exposed to predation risk may produce offspring with heightened antipredator defences. At the same time, organisms can gain information about the environment horizontally, from conspecifics. In this study, we provide some of the first evidence that horizontally acquired social information can be transmitted vertically across generations. Three-spined stickleback (Gasterosteus aculeatus) fathers produced larval offspring with altered antipredator behaviour when fathers received visual and olfactory cues from predator-chased neighbours. Although fathers did not personally witness their neighbours being chased (i.e. they never saw the predator), changes in offspring traits were similar to those induced by direct paternal exposure to predation risk. These findings suggest that two different non-genetic pathways (horizontal transfer of social information, vertical transfer via sperm-mediated paternal effects) can combine to affect offspring phenotypes. The implications of simultaneous horizontal and vertical transmission are widely appreciated in the context of disease and culture; our results suggest that they could be equally important for the maintenance of phenotypic variation and could have profound consequences for the rate at which information flows within and across generations.