The evolution of signalling and eavesdropping in plant-fungal networks

Abstract

AbstractExperiments have shown that when one plant is attacked by a pathogen or herbivore, this can lead to other plants connected to the same mycorrhizal network upregulating their defence mechanisms. It has been hypothesised that this represents signalling, with attacked plants producing a signal to warn other plants of impending harm. We examined the evolutionary plausibility of this and other hypotheses theoretically. We found that the evolution of plant signalling about an attack requires restrictive conditions, and so will rarely be evolutionarily stable. The problem is that signalling about an attack provides a benefit to competing neighbours, even if they are kin, and so reduces the relative fitness of signalling plants. Indeed, selection is often more likely to push plant behaviour in the opposite direction – with plants signalling dishonestly about an attack that has not occurred, or by suppressing a cue that they have been attacked. Instead, we show that there are two viable alternatives that could explain the empirical data: (1) the process of being attacked leads to a cue (information about the attack) which is too costly for the attacked plant to fully suppress; (2) mycorrhizal fungi eavesdrop on their host plants, detect when they are attacked, and then the fungi signal this information to warn other plants in their network. Our results suggest the empirical work that would be required to distinguish between these possibilities.Significance statementExperiments have shown that when one plant is attacked by a herbivore, this can lead to other plants connected to the same mycorrhizal network upregulating their defence mechanisms. It has been hypothesised that this represents signalling, with attacked plants producing a signal to warn other plants of impending harm. We found theoretically that plant warning signals are rarely evolutionarily stable. Instead, we identify two viable alternatives that could explain the empirical data: (1) being attacked leads to a cue (information about the attack) which is too costly for the attacked plant to suppress; (2) mycorrhizal fungi eavesdrop on their host plants, detect when they are attacked, and then the fungi signal this information to warn other plants in their network.