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Abstract Understanding the often antagonistic plant–herbivore interactions and how host defenses can influence herbivore dietary breadth is an area of ongoing study in ecology and evolutionary biology. Typically, host plants/fungi that produce highly noxious chemical defenses are only fed on by specialists. We know very little about generalist species that can feed and develop on a noxious host. One such example of generalists feeding on toxic host occurs in the mushroom‐feedingDrosophilafound in theimmigrans‐tripunctataradiation. Although these species are classified as generalists, their acceptable hosts include deadlyAmanitaspecies. In this study, we used behavioral assays to assess associations between one mushroom‐feeding species,Drosophila guttifera, and the deadlyAmanita phalloides. We conducted feeding assays to confirm the presence of cyclopeptide toxin tolerance. We then completed host preference assays in female flies and larvae and did not find a preference for toxic mushrooms in either. Finally, we assessed the effect of competition on oviposition preference. We found that the presence of a competitor's eggs on the preferred host was associated with the flies increasing the number of eggs laid on the toxic mushrooms. Our results highlight how access to a low competition host resource may help to maintain associations between a generalist species and a highly toxic host. 

Abstract Understanding how and when key novel adaptations evolved is a central goal of evolutionary biology. Within theimmigrans‐tripunctataradiation ofDrosophila, many mushroom‐feeding species are tolerant of host toxins, such as cyclopeptides, that are lethal to nearly all other eukaryotes. In this study, we used phylogenetic and functional approaches to investigate the evolution of cyclopeptide tolerance in theimmigrans‐tripunctataradiation ofDrosophila. First, we inferred the evolutionary relationships among 48 species in this radiation using 978 single copy orthologs. Our results resolved previous incongruities within species groups across the phylogeny. Second, we expanded on previous studies of toxin tolerance by assaying 16 of these species for tolerance to α‐amanitin and found that six of them could develop on diet with toxin. Finally, we asked how α‐amanitin tolerance might have evolved across theimmigrans‐tripunctataradiation, and inferred that toxin tolerance was ancestral in mushroom‐feedingDrosophilaand subsequently lost multiple times. Our findings expand our understanding of toxin tolerance across theimmigrans‐tripunctataradiation and emphasize the uniqueness of toxin tolerance in this adaptive radiation and the complexity of biochemical adaptations. 

Abstract The bacterial gut microbiota of many animals is known to be important for many physiological functions including detoxification. The selective pressures imposed on insects by exposure to toxins may also be selective pressures on their symbiotic bacteria, who thus may contribute to the mechanism of toxin tolerance for the insect. Amatoxins are a class of cyclopeptide mushroom toxins that primarily act by binding to RNA polymerase II and inhibiting transcription. Several species of mycophagousDrosophilaare tolerant to amatoxins found in mushrooms of the genusAmanita, despite these toxins being lethal to most other known eukaryotes. These species can tolerate amatoxins in natural concentrations to utilize toxic mushrooms as larval hosts, but the mechanism by which these species are tolerant remains unknown. Previous data have shown that a local population ofD. tripunctataexhibits significant genetic variation in toxin tolerance. This study assesses the potential role of the microbiome in α‐amanitin tolerance in six wild‐derived strains ofDrosophila tripunctata. Normal and antibiotic‐treated samples of six strains were reared on diets with and without α‐amanitin, and then scored for survival from the larval stage to adulthood and for development time to pupation. Our results show that a substantial reduction in bacterial load does not influence toxin tolerance in this system, while confirming genotype and toxin‐specific effects on survival are independent of the microbiome composition. Thus, we conclude that this adaptation to exploit toxic mushrooms as a host is likely intrinsic to the fly's genome and not a property of their microbiome. 

Abstract Understanding plant‐insect interactions is an active area of research in both ecology and evolution. Much attention has been focused on the impact of secondary metabolites in the host plant or fungi on these interactions. Plants and fungi contain a variety of biologically active compounds, and the secondary metabolite profile can vary significantly between individual samples. However, many experiments characterize the biological effects of only a single secondary metabolite or a subset of these compounds.Here, we develop an exhaustive extraction protocol using an accelerated solvent extraction protocol to recover the complete suite of cyclopeptides and other secondary metabolites found inAmanita phalloides(death cap mushrooms) and compare its efficacy to the “Classic” extraction method used in earlier works.We demonstrate that our extraction protocol recovers the full suite of cyclopeptides and other secondary metabolites inA. phalloidesunlike the “Classic” method that favors polar cyclopeptides.Based on these findings, we provide recommendations for how to optimize protocols to ensure exhaustive extracts and also the best practices when using natural extracts in ecological experiments.