Transgenerational non-genetic inheritance has fitness costs and benefits under recurring stress in the clonal duckweed Spirodela polyrhiza

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.

Transgenerational competition effects persist across multiple generations and are altered by offspring competitive environments in a clonal plant

“…Under this less‐crowded environment, plants may produce, for example, larger but thinner leaves to capture lights more efficiently (Puglielli et al, 2017; Zhang et al, 2020). Moreover, these adaptive responses to environmental stresses may be accumulative over the course of multiple generations and thus crucial for the structures and dynamics of plant populations (e.g., Herman et al, 2012; Huber et al, 2021; Miao et al, 1991). For instance, Herman et al (2012) found that when both grandparent and parent were drought stressed, the offspring could achieve greater root growth than when either the grandparental or parental generation alone was drought stressed.…”

Parental effects driven by resource provisioning in Alternanthera philoxeroides—A simulation case study

“…During the entire life cycle of clonal plants, clonal offspring ramets are repeatedly produced by parental ramets, so the performance of offspring ramets is greatly influenced by the environments that parental ramets have encountered ( Latzel and Klimešová, 2010 ; Douhovnikoff and Dodd, 2015 ). An increasing body of evidence has documented that parental environments may to some extent regulate the survival, early development, and subsequent growth of clonal offspring across vegetative generations, and also adjust the life-history strategy of clonal offspring to pre-adapt to future environments ( González et al, 2016 , 2017 ; Münzbergová and Hadincová, 2017 ; Dong et al, 2019a , b ; DuBois et al, 2020 ; Huber et al, 2021 ). Compared to sexually reproducing plants, such parental environmental effects are especially important for clonal plants with a low potential for adaptation through genetically based natural selection.…”

“…In addition, the magnitude of parental effects may fluctuate at the different developmental stages of clonal offspring ( Schwaegerle et al, 2000 ; Huber et al, 2021 ). Provided that parental effects are mainly regulated by the provisioning of resources, such kind of parental effects are predicted to play a key role for clonal offspring at the early developmental stage than at the late stage ( Schwaegerle et al, 2000 ).…”

Editorial: Ecoepigenetics in clonal and inbreeding plants: Transgenerational adaptation and environmental variation, Volume II

“…Recent work suggests that the performance of an individual (ramet) of clonal plants is influenced by not only its current environmental condition but also the environmental condition of its parents ( Huber et al., 2021 ; Xue et al., 2022 ). At least three mechanisms can explain such transgenerational (parental or maternal) effects ( Herman and Sultan ; Luo et al., 2022 ).…”

“…Long-lived clonal plants, in which reproduction is mainly asexual and clonal growth plays a central role in their population spread and maintenance, have long been thought to possess low genetic variation so that the potential for genetics-based adaptation to environmental changes may be limited. Thus, epigenetic variation may be particularly important for these clonal plants to adapt to rapid environmental changes (Latzel and Klimesǒva, 2010;Dodd and Douhovnikoff;Mounger et al, 2021).Recent work suggests that the performance of an individual (ramet) of clonal plants is influenced by not only its current environmental condition but also the environmental condition of its parents (Huber et al, 2021;Xue et al, 2022). At least three mechanisms can explain such transgenerational (parental or maternal) effects (Herman and Sultan;Luo et al, 2022).…”