Cheating emergences in the arbuscular mycorrhizal mutualism: a network and phylogenetic analysis

Abstract

O_LIWhile mutualisms are widespread and essential in ecosystem functioning, the emergence of uncooperative cheaters threatens their stability, unless there are functional or evolutionary mechanisms limiting cheaters interactions.\nC_LIO_LIHere, we evaluated the constraints upon mycoheterotrophic (MH) cheating plants in the mutualistic interaction network of autotrophic (AT) plants and arbuscular mycorrhizal fungi. For this purpose, we assembled a world-scale network of >25,000 interactions in order to investigate (i) the specialization and (ii) the phylogenetic distribution of MH or AT plants and their respective fungal partners.\nC_LIO_LIWe show that MH cheating repeatedly evolved in the vascular flora, suggesting low phylogenetic constraint for plants. However, MH cheaters are significantly more specialized than AT plants, and their fungi also appear more specialized and more closely related than fungi of AT plants, which suggest that cheaters are specifically isolated into modules by functional constraints\nC_LIO_LIThis unprecedented comparison of MH vs. AT plants thus reveals that MH cheating is most likely constrained by the specialization of phylogenetically conserved cheating-susceptible fungi, which suggests mechanisms for avoidance of these fungi. Beyond the mycorrhizal symbiosis, our approach highlights an empirical multiple-partners mutualistic system illustrating that the overall persistence of mutualism can be linked to functional constraints upon cheating emergences.\nC_LI