Unveiling the evolutionary and ecological effects of transgenerational plasticity in monoclonal giant duckweeds
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Abstract
Recent studies have demonstrated that stress experienced by previous generations can
influence the phenotype of their descendants, yet its impact on fitness and adaptability remains
unclear. To investigate this, we exposed multiple genotypes of the clonal giant duckweed
(Spirodela polyrhiza) to copper excess and herbivory by the waterlily aphid (Rhopalosiphum
nymphaeae) over five generations. After another five generations without stress, we
reintroduced both abiotic and biotic stressors under laboratory and natural conditions. Through
ancestral exposure to copper excess in 56 globally distributed genotypes grown under axenic
conditions and minimized natural selection, we found consistent evidence that
transgenerational plasticity is heritable, reproducible, and dependent on both genotype and
environment. The trade-offs of this plasticity could be predicted by the initial resistance of the
plants to stress, likely due to resource allocation. Physiological analysis revealed that ancestral
copper excess increased cyanidin concentrations, likely protecting photosystem II efficiency.
These findings suggest that transgenerational plasticity is regulated by genes involved in plant
reproduction and defence. Additionally, plants exposed to ancestral copper excess boosted
aphid fitness. Unexpectedly, copper-induced transgenerational jasmonates, when
supplemented to plants, benefitted the waterlily aphid, demonstrating that copper-induced
transgenerational plasticity can affect interacting species. Similarly, ancestral aphid herbivory
led to maladaptive effects under recurring herbivory, further increasing aphid reproduction.
Metabolomic and transcriptomic analyses revealed that, in addition to increased jasmonates,
aphid herbivory transgenerationally induced the accumulation of tyramine through regulation
of its biosynthetic machinery. Supplementation of tyramine to plants and aphids confirmed its
adaptive role against herbivory. Under natural conditions, tyramine, but not jasmonates,
exhibited transgenerational plasticity over two consecutive years, and accordingly, aphid
fitness tended to decline outdoors, highlighting the relevance of executing experiments under
both laboratory and natural conditions. Together, these findings demonstrate that
transgenerational plasticity is heritable and plays a crucial role in organismal and community
evolutionary change, as it not only shapes the fitness and phenotype of the affected organisms
but also impacts coexisting species under both controlled and natural conditions.