The specificity of sperm-mediated paternal effects in threespine sticklebacks

Abstract: Parental effects may help offspring respond to challenging environments, but whether parental exposure to different environmental challenges induces similar responses in offspring is largely unknown. We compared the offspring of threespine stickleback (Gasterosteus aculeatus) fathers who had been exposed to a potentially threatening stimulus (net), a native predator (sculpin), or who had been left unexposed (control). Relative to offspring of control fathers, offspring of sculpin-exposed fathers were more responsive (greater change in activity) to a simulated sculpin predator attack, while offspring of net-exposed fathers were less responsive (fewer antipredator behaviors) and showed altered stress responses compared to the control. To evaluate whether parental exposure primes offspring to respond to specific stimuli (e.g., offspring of net-exposed fathers respond most strongly to a net), we then exposed offspring of each paternal treatment to nets, native sculpin models, or non-native trout models. Paternal treatment did not influence offspring response to different stimuli; instead, offspring were generally more responsive to the native sculpin predator compared to nets or non-native trout predator, suggesting that sticklebacks have innate predator recognition of native predators. Collectively, these results underscore that, while parental exposure to non-ecologically relevant stressors elicits effects in intergenerational studies, these findings may not mirror those produced when parents encounter ecologically relevant stressors. Knowing that parental effects can be predator-specific furthers our understanding of the ways in which parental effects may evolve to be adaptive and suggests the potential for transgenerational plasticity to affect how animals respond to human induced environmental change, including non-native predators. Significance statement: Despite extensive evidence for parental effects, we have very little knowledge regarding whether parental effects are stimuli-specific. Here, we found that paternal exposure to different, potentially stressful stimuli prior to fertilization has specific effects on offspring traits: paternal exposure to a model of a sculpin (a native predator) heightened offspring responsivity to simulated predation risk, while paternal exposure to an artificial stimulus/stressor (net) reduced offspring antipredator behavior relative to the control. We found no evidence that offspring responded more strongly to the stimulus that their father encountered; instead, offspring were overall more responsive to a sculpin predator compared to a net or non-native trout. Overall, these results suggest that sperm-mediated paternal effects can be highly specific, and while non-ecologically relevant stimuli elicit effects in intergenerational studies, these effects may differ from those that occur when parents are exposed to native, ecologically relevant stimuli.