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

Indirect ecological interactions are thought to be ubiquitous in nature
and may be important in shaping evolutionary processes in multitrophic
communities. However, direct evidence of indirect interactions driving
evolutionary processes is still lacking. Here, we characterized how the
indirect effects of terrestrial insect (aphids) herbivory on macrophytes
(duckweed) affected the evolution of an aquatic community using real-time
evolutionary experiments in a two-year outdoor pond experiment. Aphid
herbivory reduced macrophyte growth and increased the abundance of
phytoplankton, which in turn increased the abundance of zooplankton
consumers. Pool sequencing and phenotypic assays showed that the aphid
herbivory altered the genetic compositions of Daphnia magna populations, a
key member of the zooplankton community. In the second year, transplant
experiments further indicated that evolutionary changes in D. magna driven
by the aphid herbivory on the macrophytes were adaptive and that changes
in the aquatic community altered aphid-macrophyte interactions. These
results suggest that indirect ecological interactions can shape
eco-evolutionary dynamics in multitrophic communities.