Maladaptive aphid-induced transgenerational plasticity is overcome in nature

Transgenerational plasticity is widely presumed adaptive, yet empirical evidence is scarce, especially in natural conditions. Using the clonally reproducing giant duckweed (Spirodela polyrhiza) and its native herbivore, the waterlily aphid (Rhopalosiphum nymphaeae), we show that herbivores benefit from plant transgenerational plasticity. In monoclonal, single-descendant lineages indoors, duckweed supported higher aphid reproduction and suffered decreased fitness when their ancestors encountered aphids five generations earlier. Gene expression and metabolite profiling suggest transgenerational priming as underlying mechanism: duplicated L-tyrosine decarboxylase genes elevated tyramine levels, an adaptive response as tyramine supplementation suppressed aphid reproduction. Contrary, transgenerational jasmonate priming was maladaptive, as methyl-jasmonate application enhanced aphid reproduction. Remarkably, in a two-year outdoor mesocosm experiment with monoclonal S. polyrhiza populations of up to one million individuals, transgenerational tyramine priming persisted, whereas transgenerational jasmonate priming and its costs disappeared. These findings indicate that herbivores can hijack plant transgenerational plasticity, but that natural environments may counteract such changes.