Ecological context determines whether inherited stress responses of hosts benefit or harm herbivores

Inherited stress responses are widely assumed to be adaptive for plants by preparing offspring for renewed attack. To date, it remains unclear whether and under which conditions these responses may benefit the attacker rather than the host. Studying the interaction between the aphid Rhopalosiphum nymphaeae and its native host, the aquatic duckweed Spirodela polyrhiza , we show that aphids can either benefit or suffer from inherited stress responses, depending on metabolite identity and ecological context. In multigenerational clonal plant lineages maintained indoors, ancestral aphid herbivory increased aphid reproduction and reduced plant fitness under renewed attack, indicating that the net effect of inherited stress responses can favor the herbivore. However, not all inherited responses benefited the aphid: using genetic and chemical manipulations, we found that transgenerational priming of jasmonate enhanced aphid performance, whereas transgenerational priming of tyramine reduced it. Notably, tyramine—but not jasmonates—accumulated to higher levels across generations also in large mesocosms outdoors, albeit only within and not across growing seasons. Together, our results reveal that inherited responses of hosts can favor the attackers and highlight ecological context and life-cycle transitions as key determinants of the persistence, duration, and ecological consequences of inherited stress responses.