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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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Examining the associations between a generalist feeder and a highly toxic host
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.
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- PAR ID:
- 10492169
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Ecology and Evolution
- Volume:
- 14
- Issue:
- 2
- ISSN:
- 2045-7758
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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Abstract Background The recognition and delineation of morphologically indistinguishable cryptic species can have broad implications for wildlife conservation, disease ecology and accurate estimates of biodiversity. Parasites are intriguing in the study of cryptic speciation because unique evolutionary pressures and diversifying factors are generated by ecological characteristics of host-parasite relationships, including host specificity. Bat flies (Diptera: Nycteribiidae and Streblidae) are obligate, hematophagous ectoparasites of bats that generally exhibit high host specificity. One rare exception is Penicillidia fulvida (Diptera: Nycteribiidae), an African bat fly found in association with many phylogenetically distant hosts. One explanation for P. fulvida ’s extreme polyxeny is that it may represent a complex of host-specific yet cryptic species, an increasingly common finding in molecular genetic studies of supposed generalist parasites. Methods A total of 65 P. fulvida specimens were collected at 14 localities across Kenya, from bat species representing six bat families. Mitochondrial cytochrome c oxidase subunit 1 ( COI ) and nuclear 28S ribosomal RNA (rRNA) sequences were obtained from 59 specimens and used to construct Bayesian and maximum likelihood phylogenies. Analysis of molecular variance was used to determine how genetic variation in P. fulvida was allocated among host taxa. Results The 28S rRNA sequences studied were invariant within P. fulvida . Some genetic structure was present in the COI sequence data, but this could be more parsimoniously explained by geography than host family. Conclusions Our results support the status of P. fulvida as a rare example of a single bat fly species with primary host associations spanning multiple bat families. Gene flow among P. fulvida utilizing different host species may be promoted by polyspecific roosting behavior in bats, and host preference may also be malleable based on bat assemblages occupying shared roosts. The proclivity of generalist parasites to switch hosts makes them more likely to vector or opportunistically transmit pathogens across host species boundaries. Consequently, the presence of polyxenous bat flies is an important consideration to disease ecology as bat flies become increasingly known to be associated with bat pathogens. Graphical Abstractmore » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1002/ece3.11035
