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Species interactions are a unifying theme in ecology and evolution. Both fields are currently moving beyond their historical focus on isolated pairwise relationships to understand how ecological communities affect focal interactions. Additional species can modify both the number of interactions and the fitness consequences of each interaction (i.e., selection). Although only selection affects the evolution of the focal interaction, the two are often conflated, limiting our understanding of the evolution of multispecies interactions. We manipulated aboveground herbivory on the legume Medicago lupulina in the field and quantified its effect on number of symbionts and the per-symbiont impact on plant performance in two belowground symbioses: mutualistic rhizobia bacteria (Ensifer meliloti) and parasitic root-knot nematodes (Meloidogyne hapla). We found that herbivores modified the number of rhizobia nodules, as well as the benefit per nodule. However, each effect was specific to a distinct herbivory regime: natural herbivory affected nodule number, whereas leafhoppers (Cicadellidae) weakened the per nodule benefit. We did not detect any effect of herbivory on nematode gall number or the cost of infection. Our data demonstrate that distinguishing between symbiont number from the fitness consequences of symbiosis is crucial to accurately infer how pairwise interactions will evolve in a community.

Priority effects shape the assembly of free-living communities and host-associated communities. However, the current literature does not fully incorporate two features of host-symbiont interactions, correlated host responses to multiple symbionts and ontogenetic changes in host responses to symbionts, leading to an incomplete picture of the role of priority effects in host-associated communities. We factorially manipulated the inoculation timing of two plant symbionts (mutualistic rhizobia bacteria and parasitic root-knot nematodes) and tested how host age at arrival, arrival order, and arrival synchrony affected symbiont colonization success in the model legume Medicago truncatula. We found that host age, arrival order, and arrival synchrony significantly affected colonization of one or both symbionts. Host age at arrival only affected nematodes but not rhizobia: younger plants were more heavily infected than older plants. By contrast, arrival order only affected rhizobia but not nematodes: plants formed more rhizobia nodules when rhizobia arrived before nematodes. Finally, synchronous arrival decreased colonization both symbionts, an effect that depended on host age. Our results demonstrate that priority effects compromise the host's ability to control colonization by two major symbionts and suggest that the role of correlated host responses and host ontogeny in the assembly of host-associated communities deserve further attention.