Abstract
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.
Highlights
Dwindling intraspecific genetic diversity in both natural and agroecosystems due to human practices has fuelled interest in the ability of species to resist environmental change in the absence of genetic variation through non-genetic inheritance
The importance of non-genetic inheritance is a major controversy in plant ecology and evolution [7,22,42,43,44], because fitness costs and benefits of transgenerational stress response across multiple generations are often unclear
By directly estimating plant fitness in the clonal freshwater plant S. polyrhiza, we showed that copper excess may modulate offspring fitness for up to 10 generations after stress release, and the adaptiveness of the observed responses depended on the genotype, the duration of the stress exposure and the interval between initial and recurring conditions
Summary
Dwindling intraspecific genetic diversity in both natural and agroecosystems due to human practices has fuelled interest in the ability of species to resist environmental change in the absence of genetic variation through non-genetic inheritance. Theoretical work suggests that populations may acquire stress resistance through non-genetic inheritance, when transmission fidelity across generations is high [8,9] Experimental support of these predictions in multicellular organisms is, scarce [6,10,11], as such approaches require large-scale multi-generational studies and the ability to disentangle genetic from non-genetic factors [12]. Directly assessing plant fitness when initial and recurring stress are separated by multiple generations is critical to progress our understanding of the ecological and evolutionary implications of non-genetic inheritance. Our results demonstrate that depending on the genotype and the interval that separated initial and recurring conditions, copper excess may have positive, negative or neutral effects on offspring fitness and may modulate plant copper and flavonoid accumulation. This study thereby highlights the importance and context dependency of non-genetic inheritance for plant ecology and evolution
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