Neopolyploidy-induced changes in the giant duckweed (Spirodela polyrhiza) alter herbivore preference, performance, and plant population performance

Abstract

PremisePolyploidy is a widespread mutational process in angiosperms that may alter population performance of not only plants but also their animal associates. Yet, knowledge of whether ploidy affects plant-herbivore dynamics is scarce. Here, we test whether aphid herbivores exhibit preference for diploid or neopolyploid plants, whether ploidy impacts plant and herbivore performance, and whether these interactions depend on plant genetic background.MethodsUsing multiple pairs of independently synthesized neotetraploid greater duckweed (Spirodela polyrhiza) and their diploid progenitors, we evaluated the effect of neopolyploidy on duckweed’s interaction with the water-lily aphid (Rhopalosiphum nymphaeae). Using two-way choice experiments, we first evaluated feeding preference by the herbivore. We then evaluated the consequences of ploidy on aphid and plant performance by measuring population growth over multiple generations.Key ResultsAphids preferred neopolyploids over diploids when the plants were provided at equal abundances but not when they were provided at equal surface area, indicating the role of plant size in driving this preference. Additionally, neopolyploidy increased aphid population performance, but this result was highly dependent on the genetic lineage of the plant. Lastly, the impact of herbivory on neopolyploids vs. diploid duckweed varied greatly with genetic lineage, but overall, neopolyploids appeared to be generally less tolerant than diploids.ConclusionsWe conclude that polyploidization can impact the preference and performance of herbivores on their plant hosts, whereas plant performance depends on complex interactions between herbivory, ploidy, and genetic lineage. These results have significant implications for the establishment and persistence of plants and herbivores in nature.

Neopolyploidy increases stress tolerance and reduces fitness plasticity across multiple urban pollutants: support for the “general-purpose” genotype hypothesis

“…Our results demonstrated that stress conditions can upend fitness differences between the ploidies. Large diploid population growth advantages under favorable (control) conditions ( Figures 1 and 2 ) corroborate previous studies with synthetic neopolyploid duckweeds ( Anneberg et al, 2023a ; Assour et al, 2023 ). However, here we showed that when exposed to pollutant stress, diploids were more similar to polyploids, and one contaminant (copper) even reversed the direction of the diploid–neopolyploid difference.…”

“…This disconnect suggests that functional differences within diploid S. polyrhiza may derive from epigenetic variation that can be altered by autopolyploidization along with genetic variation ( Chen, 2007 ; Huber et al, 2021 ) and strongly influence stress tolerance and population growth. Regardless of the mechanism, our results join those of several others demonstrating the importance of genetic variation in diploid progenitors on neopolyploid morphology ( Wei et al, 2020 ), population growth ( Anneberg et al, 2023a ), and response to abiotic ( Bafort et al, 2023 ; Wei et al, 2020 ) and biotic interactions ( Anneberg et al, 2023b ; Assour et al, 2023 ; Forrester et al, 2020 ). They provide additional support for the idea that the repeated evolution of polyploids may be key to their success ( Kolář et al, 2017 ; Soltis & Soltis, 1999 ; Wei et al, 2020 ).…”