Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown

Significance Cooperative interactions among species—mutualisms—are major sources of evolutionary innovation. However, despite their importance, two species that formerly cooperated sometimes cease their partnership. Why do mutualisms break down? We asked this question in the partnership between arbuscular mycorrhizal (AM) fungi and their plant hosts, one of the most ancient mutualisms. We analyze two potential trajectories toward evolutionary breakdown of their cooperation, symbiont switching and mutualism abandonment. We find evidence that plants stop interacting with AM fungi when they switch to other microbial mutualists or when they evolve alternative strategies to extract nutrients from the environment. Our results show vital cooperative interactions can be lost, but only if successful alternatives evolve. Cooperative interactions among species, termed mutualisms, have played a crucial role in the evolution of life on Earth. However, despite key potential benefits to partners, there are many cases in which two species cease to cooperate and mutualisms break down. What factors drive the evolutionary breakdown of mutualism? We examined the pathways toward breakdowns of the mutualism between plants and arbuscular mycorrhizal fungi. By using a comparative approach, we identify ∼25 independent cases of complete mutualism breakdown across global seed plants. We found that breakdown of cooperation was only stable when host plants (i) partner with other root symbionts or (ii) evolve alternative resource acquisition strategies. Our results suggest that key mutualistic services are only permanently lost if hosts evolve alternative symbioses or adaptations.

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