Kropelin, G. | Search bioRxiv

bioRxiv2023

Characterizing the impact and maintenance of specialized toxin tolerance in a generalist species

Understanding how plant-herbivore interactions can drive coevolution is a central goal of ecology and evolutionary biology. Of particular interest are the defenses produced by host plants/fungi and their impact on herbivore feeding strategies. In the immigrans-tripunctata radiation of Drosophila, mushroom-feeding species are classified as generalists, but their acceptable hosts include deadly Amanita species. In this study, we used behavioral assays to assess whether the mushroom-feeding species Drosophila guttifera is becoming a specialist and to characterize the impact of competition on host usage. 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 competitors eggs on the preferred host was associated with the flies increasing the number of eggs laid on the toxic mushrooms. Our results suggest that an adaptation associated with specialized feeding behavior is not altering host usage and that competition plays a role in maintaining this trait. More broadly our work highlights how access to a low competition host resource helps to maintain adaptations with fitness costs.

evolutionary biology↗

bioRxiv2023

Investigating the phylogenetic history of toxin tolerance in mushroom-feeding Drosophila

Understanding how and when key novel adaptations evolved is a central goal of evolutionary biology. Within the immigrans-tripunctata radiation of Drosophila, 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 the immigrans-tripunctata radiation of Drosophila. We first 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 -amanitin and found that six of these species could develop on diet with toxin. Third, we examined fly development on a diet containing a natural mix of toxins extracted from the Death Cap Amanita phalloides mushroom. Both tolerant and susceptible species developed on diet with this mix, though tolerant species survived at significantly higher concentrations. Finally, we asked how cyclopeptide tolerance might have evolved across the immigrans-tripunctata radiation and inferred that toxin tolerance was ancestral and subsequently lost multiple times. Our results suggest the evolutionary history of cyclopeptide tolerance is complex, and simply describing this trait as present or absent does not fully capture the occurrence or impact on this adaptive radiation. More broadly, the evolution of novelty can be more complex than previously thought, and that accurate descriptions of such novelties are critical in studies examining their evolution.

evolutionary biology↗