Mutualist-Provided Resources Increase Susceptibility to Parasites

Background and Aims Mutualistic microbes often increase their host’s susceptibility to parasite infection, but the mechanism underlying this pattern remains unknown. We tested two competing hypotheses to identify the cause of this phenomenon. First, mutualist-provided resources could attract antagonists by making hosts more resource-rich. Second, mutualism establishment itself might increase host vulnerability to antagonists by enabling antagonists to exploit host defenses or immune systems, which are often downregulated during mutualism establishment. Methods To test which mechanism underlies increased parasite susceptibility, we experimentally decoupled mutualism establishment and mutualist-provided resources in the legume-rhizobia mutualism. We measured parasite load on Medicago truncatula plants infected with root-knot nematodes in a full-factorial design, in which we independently manipulated rhizobia inoculation (mutualism establishment) and nitrogen availability (mutualist-provided resources). Key Results Increased nitrogen availability increased parasite infection. However, its effect was non-linear and was not explained by nitrogen assimilation into plant tissues, indicating that this effect is not driven by parasite attraction to resource-rich hosts. We found little effect of mutualism establishment on susceptibility, as neither rhizobia inoculation nor nodulation without nitrogen fixation significantly increased parasite infection. Conclusions Our results suggest that mutualist-provided resources are an important driver of indirect ecological costs of mutualism, although the mechanism linking mutualist-provided resources and susceptibility to infection remains unknown.