Letters to Nature

Nature 425, 78-81 (4 September 2003) | doi:10.1038/nature01931; Received 9 May 2003; Accepted 18 July 2003

Host sanctions and the legume–rhizobium mutualism

E. Toby Kiers1, Robert A. Rousseau1, Stuart A. West2 & R. Ford Denison1

  1. Agronomy and Range Science, University of California, 1 Shields Avenue, Davis, California 95616, USA
  2. Institute of Cell, Animal & Population Biology, University of Edinburgh, King's Buildings, West Mains Road, Edinburgh EH9 3JT, UK

Correspondence to: R. Ford Denison1 Email: rfdenison@ucdavis.edu

Explaining mutualistic cooperation between species remains one of the greatest problems for evolutionary biology1, 2, 3, 4. Why do symbionts provide costly services to a host, indirectly benefiting competitors sharing the same individual host? Host monitoring of symbiont performance and the imposition of sanctions on 'cheats' could stabilize mutualism5, 6. Here we show that soybeans penalize rhizobia that fail to fix N2 inside their root nodules. We prevented a normally mutualistic rhizobium strain from cooperating (fixing N2) by replacing air with an N2-free atmosphere (Ar:O2). A series of experiments at three spatial scales (whole plants, half root systems and individual nodules) demonstrated that forcing non-cooperation (analogous to cheating) decreased the reproductive success of rhizobia by about 50%. Non-invasive monitoring implicated decreased O2 supply as a possible mechanism for sanctions against cheating rhizobia. More generally, such sanctions by one or both partners may be important in stabilizing a wide range of mutualistic symbioses.