The transgenerational consequences of paternal social isolation and predation exposure in threespined sticklebacks

Abstract

Although parents routinely encounter stress in the ecological environment that can affect offspring development (transgenerational plasticity: TGP), nearly all organisms interact with conspecifics that can either independently induce parental stress or can alter how parents respond to ecological stressors. During social buffering, the presence of conspecifics can reduce the response to or increase the speed of recovery from a stressor. This may have cascading effects on offspring if the presence of conspecifics can mitigate parental responses to ecological stress in ways that blunt transmission of stress-induced transgenerational effects. Here, we simultaneously manipulated both paternal social isolation and experience with predation risk prior to fertilization in threespined stickleback (Gasterosteus aculeatus). If social buffering mitigates TGP induced by paternal exposure to predation risk, then we expected fewer phenotypic effects in offspring when fathers are exposed to predation risk with a conspecific with present compared to fathers exposed to predation risk while isolated. Offspring of predator-exposed fathers showed reduced anxiety-like behavior. Fathers who were socially isolated had offspring that were captured faster by a live predator, suggesting that social isolation may be a stressor that has maladaptive consequences for offspring. Further, we also found evidence that the presence of a conspecific buffered fathers against the effects of predation risk: offspring of predator-exposed fathers tended to be captured faster by the predator, especially when fathers were isolated compared to when they had neighbors. Our results suggest that socially-induced stress is an important, yet underappreciated, mediator of TGP and can elicit transgenerational effects even in species that do not form permanent social groups. Future studies should therefore consider the broader social environment when predicting both within and trans-generational responses to ecological change.