Although non-genetic inheritance is thought to play an important role in plant ecology and evolution, evidence for adaptive transgenerational plasticity is scarce. Here, we investigated the consequences of copper excess on offspring defences and fitness under recurring stress in the duckweed Spirodela polyrhiza across multiple asexual generations . Growing large monoclonal populations (greater than 10 000 individuals) for 30 generations under copper excess had negative fitness effects after short and no fitness effect after prolonged growth under recurring stress. These time-dependent growth rates were likely influenced by environment-induced transgenerational responses, as propagating plants as single descendants for 2 to 10 generations under copper excess had positive, negative or neutral effects on offspring fitness depending on the interval between initial and recurring stress (5 to 15 generations). Fitness benefits under recurring stress were independent of flavonoid accumulations, which in turn were associated with altered plant copper concentrations. Copper excess modified offspring fitness under recurring stress in a genotype-specific manner, and increasing the interval between initial and recurring stress reversed these genotype-specific fitness effects. Taken together, these data demonstrate time- and genotype-dependent adaptive and non-adaptive transgenerational responses under recurring stress, which suggests that non-genetic inheritance alters the evolutionary trajectory of clonal plant lineages in fluctuating environments.

Although non-genetic inheritance is thought to play an important role in plant ecology and evolution, evidence for adaptive transgenerational responses is scarce. Here, we investigated the consequences of copper excess on offspring defense and fitness in the duckweed Spirodela polyrhiza across multiple generations. We found that descendants of large monoclonal populations (>10,000 individuals) that grew for 30 generations under copper excess exhibited negative fitness during the first few generations and positive fitness in consecutive generations under recurring stress. Similarly, propagating individual plants for 5 or 10 generations under copper excess decreased plant fitness when 5 generations and improved fitness when 10 generations passed between initial and recurring stress. Fitness benefits under recurring stress were partially associated with avoidance of excessive copper but not increased flavonoid accumulation. Taken together, these data demonstrate time-dependent adaptive transgenerational responses under recurring stress, which highlights the importance of non-genetic inheritance for plant ecology and evolution.

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