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

Abstract

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.