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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.
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Effect of gut microbiota on α‐amanitin tolerance in Drosophila tripunctata
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.
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- Award ID(s):
- 1737869
- PAR ID:
- 10442883
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 10
- Issue:
- 17
- ISSN:
- 2045-7758
- Page Range / eLocation ID:
- p. 9419-9427
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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