Boettner, L. | bioRxiv Science

bioRxiv2024

Terrestrial herbivory drives adaptive evolution in an aquatic community via indirect effects

Indirect ecological effects, which occur when the impact of one species on another is mediated by a third species or the shared environment, are ubiquitous in nature. Given the complexity of natural systems, indirect ecological effects were thought to be important in driving eco-evolutionary processes across community boundaries. However, we know remarkably little about such effects. Here we show that indirect effects of terrestrial insect (aphids) herbivory on macrophytes (duckweed) drives adaptive evolution of water fleas (Daphnia) in large outdoor aquatic mesocosms. Aphid herbivory reduced macrophyte growth and increased the abundance of phytoplankton, which in turn increased the abundance of Daphnia. Whole genome pool sequencing and phenotypic assays revealed an impact on the genetic compositions of the Daphnia populations and transplant experiments indicated that these evolutionary changes were adaptive. Furthermore, these changes in the aquatic community altered the interactions of the aphids and the macrophytes. These results demonstrate that indirect ecological effects can shape eco-evolutionary interactions between different communities.

evolutionary biology↗

bioRxiv2022

Natural rubber reduces herbivory and alters the microbiome below ground

O_LILaticifers are hypothesized to mediate both plant-herbivore and plant-microbe interactions. However, there is little evidence for the dual function of these secretory structures. C_LIO_LIWe investigated whether the major constituent of natural rubber, cis-1,4-polyisoprene, a phylogenetically widespread and economically important latex polymer, alters plant resistance and the root microbiome of the Russian dandelion (Taraxacum koksaghyz) under attack of a root herbivore, the larva of the May cockchafer (Melolontha melolontha). C_LIO_LIRubber-depleted transgenic plants lost more shoot and root biomass upon herbivory than normal rubber content near-isogenic lines. M. melolontha preferred to feed on artificial diet supplemented with rubber-depleted rather than normal rubber content latex. Likewise, adding purified cis-1,4-polyisoprene in ecologically relevant concentrations to diet deterred larval feeding and reduced larval weight gain. Metagenomics and metabarcoding revealed that abolishing biosynthesis of natural rubber alters the structure but not the diversity of the rhizosphere and root microbiota in a herbivore-dependent manner. Roots from rubber-depleted plants, however, did not exhibit a higher pathogen load compared to normal rubber content roots. C_LIO_LITaken together, our data demonstrate that natural rubber biosynthesis reduces herbivory and alters the plant microbiota in a herbivore-dependent manner, which highlights the role of plant specialized metabolites and secretory structures in shaping multitrophic interactions. C_LI

plant biology↗