Soil microbe-induced plant resistance alters aphid inter-genotypic competition leading to rapid evolution with consequences for plant growth and aphid abundance

AbstractPlants and insect herbivores are two of the most diverse multicellular groups in the world, and both are strongly influenced by interactions with the belowground soil microbiome. Effects of reciprocal rapid evolution on ecological interactions between herbivores and plants have been repeatedly demonstrated, but it is unknown if (and how) the soil microbiome could mediate these eco-evolutionary processes.We tested the role of a plant-beneficial soil bacterium (Acidovorax radicis) in altering eco-evolutionary interactions between sap-feeding aphid herbivores (Sitobion avenae) feeding on barley (Hordeum vulgare). We reared two aphid genotypes separately or together on three barley varieties that were inoculated with or without A. radicis bacteria. In the first experiment we counted the aphid number and plant biomass after 7, 14 and 21 days of aphid growth, while in a second experiment we counted and removed offspring every 1-2 days to assess aphid longevity and fecundity.Results showed that A. radicis increased plant growth and suppressed aphids of both genotypes. The strength of effect was dependent on aphid genotype and barley variety, while the direction of effect was altered by aphid population mixture. Fescue aphids experienced increased growth when they were sharing the plant with Sickte aphids on inoculated plants; this increase was not seen in the control plants without A. radicis and was only apparent after 14 days of aphid population growth.Plant inoculation with A. radicis reduced aphid survival (reduced number of reproductive days) and fecundity (reduced daily reproductive output for surviving aphids). In the second experiment, when density was controlled, Fescue aphids did not experience increased reproduction in mixed populations, suggesting this is a density-dependent effect. Using Lotka-Volterra modelling, we demonstrated that A. radicis inoculation decreased aphid population stability as it increased inter-genotype competition but decreased the intra-genotype competition (likely through reduced population density).Our work demonstrates the important role that plant-associated microbiomes can have in mediating eco-evolutionary interactions between herbivores and host plants.