Species across the tree of life rely on mutualists for key biological functions. However, many genes underlying mutualisms play a dual role in resisting parasites and pathogens, raising the intriguing possibility that susceptibility to infection is a pleiotropic cost of mutualism. Parasites often infect hosts via mechanisms that are similar to those used by mutualists, which may create a tradeoff between attracting mutualists and resisting parasites. While the significance of such genetic pleiotropy for morphological, physiological, and behavioral traits has been recognized for nearly a century, its role in species interactions remains largely overlooked. Such genetic conflict has the potential to constrain the evolution of parasite resistance and limit host investment in mutualism.
In a series of greenhouse experiments, we tested whether there is a genetic tradeoff between attracting mutualistic rhizobia and resisting parasitic nematodes in the legume Medicago truncatula. Legumes acquire nitrogen from mutualistic nitrogen-fixing bacteria (rhizobia). Like many other plants, they are also attacked by parasitic nematodes that steal nutrients. Rhizobia and nematodes form strikingly similar structures on plant roots, and molecular genetics suggests the same plant genes mediate both symbioses. In greenhouse experiments using M. truncatula genotypes sampled from wild populations in its native Mediterranean range, we experimentally inoculated plants with mutualistic rhizobia and parasitic nematodes and estimated the genetic correlation between investment in the rhizobial mutualism and susceptibility to nematode parasitism. We estimated investment in mutualism and susceptibility to parasitism by counting the unique structures rhizobia and nematodes form on plant roots (nodules and galls, respectively).
Results/Conclusions
Consistent with our prediction, we found that there is a genetic tradeoff between plant responses to rhizobia and nematodes. Plant genotypes that formed more nodules with rhizobia were more heavily infected by nematodes, indicating that susceptibility to nematodes is a cost of mutualism in Medicago. Surprisingly, we also discovered that genetic conflict with nematodes disrupts the rhizobia mutualism. Infected Medicago plants formed fewer nodules than uninfected plants. Our results suggest that genetically based tradeoffs between forming mutualisms and resisting parasites may constrain the evolution of both interactions, and could shape the assembly of host-associated microbial communities.