Abstract

Interspecific mutualisms are regarded as having evolved from antagonistic or commensalistic interactions, with most mutualisms remaining facultative but some having coevolved into obligate reciprocal dependency. Underlying mutualism is an intrinsic conflict between the parties, in that each is under selection for increased exploitation of the other. Theoretical models suggest that this conflict is a source of evolutionary instability, and that evolution of 'cheating' by one party may lead to reciprocal extinction. Here we present phylogenic evidence for reversal of an obligate mutualism: within the yucca moth complex, distinct cheater species derived from obligate pollinators inflict a heavy cost on their yucca hosts by laying their eggs but not pollinating the yucca. Phylogenetic data show the cheaters to have existed for a long time. Coexisting pollinators and cheaters are not sister taxa, supporting predictions that evolution of cheating within a single pollinator is evolutionarily unstable. Several lines of evidence support a hypothesis that host shifts preceded the reversal of obligate mutualism. Host or partner shifts is a mechanism that can provide a route of evolutionary escape among obligate mutualists in general.

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