The roles of tolerance in the evolution, maintenance and breakdown of mutualism

Naturwissenschaften. 2009 Oct;96(10):1137-45. doi: 10.1007/s00114-009-0559-0. Epub 2009 May 30.


Tolerance strategies are cost-reduction mechanisms that enable organisms to recover some of the fitness lost to damage, but impose limited or no cost on antagonists. They are frequently invoked in studies of plant-herbivore and of host-parasite interactions, but the possible roles of tolerance in mutualism (interspecific cooperation) have yet to be thoroughly examined. This review identifies candidate roles for tolerance in the evolution, maintenance and breakdown of mutualism. Firstly, by reducing the cost of damage, tolerance provides a key pathway by which pre-mutualistic hosts can reduce the cost of association with their parasites, promoting cooperation. This holds for the evolution of 'evolved dependency' type mutualism, where a host requires an antagonist that does not direct any reward to their partner for some resource, and of 'outright mutualism', where participants directly trade benefits. Secondly, in outright mutualism, tolerance might maintain cooperation by reducing the cost of a persisting negative trait in a symbiotic partner. Finally, the evolution of tolerance might also provide a pathway out of mutualism because the host could evolve a cheaper alternative to continued cooperation with its mutualistic partner, permitting autonomy. A key consequence of tolerance is that it contrasts with partner choice mechanisms that impose large costs on cheats, and I highlight understanding any trade-off between tolerance and partner choice as an important research topic in the evolution of cooperation. I conclude by identifying tolerance as part of a more general phenomenon of co-adaptation in mutualism and parasitism that drives the evolution of the cost/benefit ratio from the interaction.

Publication types

  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Animals
  • Ants / physiology
  • Evolution, Molecular*
  • Flowers / physiology
  • Host-Parasite Interactions / genetics
  • Models, Biological
  • Moths / physiology
  • Parasites / genetics
  • Parasites / physiology
  • Pheromones / physiology
  • Plants / parasitology
  • Pollination
  • Signal Transduction
  • Symbiosis / physiology
  • Wasps / physiology


  • Pheromones