A major conundrum in evolutionary biology is that directional selection is predicted to reduce genetic variation, yet many systems maintain high levels of variation.  Ecologists have long-looked to indirect ecological effects among suites of species as a mechanism allowing coexistence of species within communities, but the evolutionary implications of such effects remain relatively unexplored.  We used the community of bacteria, protozoa, and mosquito larvae that exists within the water-filled leaves of pitcher plants (Sarracenia purpurea) to follow the evolution of a suite of traits in one species of protozoa (Colpoda sp.) in response to direct and indirect ecological effects.  For 20 days, replicate populations of Colpoda were exposed to different selection regimes: (a) monoculture, (b) with mosquito larvae predators, (c) with a competing species of protozoa, and (d) with predators and competitors.  Following selection, we measured six traits in a common environment to determine which traits had evolved under each selection regime.

Results/Conclusions

Decreased cell size and faster cell division rate evolved in Colpoda populations in response to predation by mosquito larvae.  Decreased cell size and increased refuge use evolved in environments with competitors.  Although predators and competitors both selected for decreased cell size, environments with both species showed no evolution of cell size.  This suggests that evolution in response to indirect effects was strong and opposed to responses to direct effects.  Predation decreased competitor abundance, increased refuge use by the competitor, and altered the nature of selection on Colpoda cell size.  Perhaps more interestingly, variance in cell size predictably decreased relative to controls in response to direct selection by predation and competition, but variance was maintained in treatments with indirect effects.  Indirect ecological effects can maintain trait variation within a population, even when multiple direct effects show a pattern of directional selection, by reducing direct selection from multiple species.  Given the documented prevalence of indirect ecological effects in natural communities, we expect their evolutionary effects to be widespread, but unappreciated.