Genetic conflict with a parasitic nematode disrupts the legume-rhizobia mutualism

Abstract

Genetic variation for partner quality in mutualisms is an evolutionary paradox. One possible resolution to this puzzle is that there is a tradeoff between partner quality and other fitness-related traits. Here, we tested whether a susceptibility to parasitism is one such tradeoff in the mutualism between legumes and nitrogen-fixing bacteria (rhizobia). We performed two greenhouse experiments with the legume Medicago truncatula. In the first, we inoculated each plant with the rhizobia Ensifer meliloti and with one of 40 genotypes of the parasitic root-knot nematode Meloidogyne hapla. In the second experiment, we inoculated all plants with rhizobia and half of the plants with a genetically variable population of nematodes. Using the number of nematode galls as a proxy for infection severity, we found that plant genotypes differed in susceptibility to nematode infection, and nematode genotypes differed in infectivity. Second, we showed that there was a genetic correlation between the number of mutualistic structures formed by rhizobia (nodules) and the number of parasitic structures formed by nematodes (galls). Finally, we found that nematodes disrupt the rhizobia mutualism: nematode-infected plants formed fewer nodules and had less nodule biomass than uninfected plants. Our results demonstrate that there is genetic conflict between attracting rhizobia and repelling nematodes in Medicago. If genetic conflict with parasitism is a general feature of mutualism, it could account for the maintenance of genetic variation in partner quality and influence the evolutionary dynamics of positive species interactions.\n\nImpact summaryCooperative species interactions, known as mutualisms, are vital for organisms from plants to humans. For example, beneficial microbes in the human gut are a necessary component of digestive health. However, parasites often infect their hosts via mechanisms that are extraordinarily similar to those used by mutualists, which may create a tradeoff between attracting mutualists and resisting parasites. In this study, we investigated whether this tradeoff exists, and how parasites impact mutualism function in the barrelclover Medicago truncatula, a close relative of alfalfa. Legumes like Medicago depend on nitrogen provided by mutualistic bacteria (rhizobia) to grow, but they are also infected by parasitic worms called nematodes, which steal plant nutrients. Both microorganisms live in unique structures (nodules and galls) on plant roots. We showed that the benefits of mutualism and the costs of parasitism are predicted by the number of mutualistic structures (nodules) and the number of parasitic structures (galls), respectively. Second, we found that there is a genetic tradeoff between attracting mutualists and repelling parasites in Medicago truncatula: plant genotypes that formed more rhizobia nodules also formed more nematode galls. Finally, we found that nematodes disrupt the rhizobia mutualism. Nematode-infected plants formed fewer rhizobia nodules and less total nodule biomass than uninfected plants. Our research addresses an enduring evolutionary puzzle: why is there so much variation in the benefits provided by mutualists when natural selection should weed out low-quality partners? Tradeoffs between benefits provided by mutualists and their susceptibility to parasites could resolve this paradox.