Reversal of mutualism as a mechanism for adaptive radiation in yucca moths

Species interactions are a major source of adaptive radiation. In mutualisms, such diversification can take the form of evolution of parasites that exploit the resources needed for maintenance of the mutualism. Mutualistic associations often have associated parasitic species, and in some cases, parasitic species have indeed evolved from the mutualists. For example, obligate mutualisms, such as those involving seed-eating pollinators, have on a few occasions given rise to nonmutualist species. These systems are relatively simple and provide models for identifying factors that facilitate the stable reversal of a mutualistic interaction. We used ecological data in a phylogenetic framework to analyze the origins of two nonmutualist cheater yucca moths. Phylogenetic analysis suggests that the evolution of cheating may be preceded by a change in oviposition behavior. Two different modes of oviposition among math species cause density-dependent moth egg mortality through flower abscission in one case (locule-ovipositing species) but density-independent mortality in the other (superficially ovipositing species). A mtDNA-based phylogeny indicated that cheating and superficial oviposition have evolved twice each and that the cheater clades are sisters to the superficially ovipositing species clades. Consideration of the fitness consequences of two trait changes-loss of pollination and phenological delay in oviposition-in which cheaters have diverged from ancestral pollinators suggest that the shift to oviposition into fruit may have occurred first and that loss of pollination behavior was a secondary event. We suggest that secondary coexistence of two pollinator species of opposite oviposition modes may facilitate the shift to fruit oviposition and cheating and that this is applicable in the best documented of the cheater lucca moths. Superficially ovipositing species suffer dual sources of egg mortality when in coexistence with locule-ovipositing species. Shift to fruit oviposition under this circumstance can be facilitated by access to a seed resource not available to the copollinator, preadaptations in ovipositor morphology, and pollinator phenology late relative to the copollinator. Thus the adaptive radiation of nonmutualists from mutualists may have taken place in specific ecological contexts through few trait changes, and the reversal of mutualism would be a by-product of a shift to reliance on a previously inaccessible seed resource.