Explaining the persistence of mutualism remains a challenge in ecology and evolutionary biology. The evolutionary stability of arbuscular mycorrhiza, a most widespread and ancient mutualistic association, is particularly intriguing because plants lack apparent mechanisms to prevent cheaters from gaining competitive advantages over cooperators. We developed a triple isotopic labeling method (14C, 32P, and 33P) within a split-root design to measure the exchange of carbon (C) and phosphorus (P) between the host plant and two mycorrhizal partners across a soil P gradient. Host plant preferentially allocated more C to the roots associated with the fungus delivering higher P per unit plant C, and the strength of preferential allocation decreased with increasing soil P availability. The host plant received more P per unit of allocated C from the better fungus and this advantageous exchange rate did not depend upon P availability. As a result, the level of preferential allocation was correlated with the differential delivery of P from the two fungi. Our findings suggest that plant preferential allocation to better mutualists can stabilize mutualisms in environments limiting in the traded resource, but as the availability of this resource increases, plant preferential allocation declines. This environmental dependence of preferential allocation generates predictions of declining levels in relative abundance of mutualistic fungi in high-resource environments.
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