A phylogenomic analysis of lichen-feeding tiger moths uncovers evolutionary origins of host chemical sequestration.

Host species utilize a variety of defenses to deter feeding, including secondary chemicals. Some phytophagous insects have evolved tolerance to these chemical defenses, and can sequester secondary defense compounds for use against their own predators and parasitoids. While numerous studies have examined plant-insect interactions, little is known about lichen-insect interactions. Our study focused on reconstructing the evolution of lichen phenolic sequestration in the tiger moth tribe Lithosiini (Lepidoptera: Erebidae: Arctiinae), the most diverse lineage of lichen-feeding moths, with 3000 described species. We built an RNA-Seq dataset and examined the adult metabolome for the presence of lichen-derived phenolics. Using the transcriptomic dataset, we recover a well-resolved phylogeny of the Lithosiini, and determine that the metabolomes within species are more similar than those among species. Results from an initial ancestral state reconstruction suggest that the ability to sequester phenolics produced by a single chemical pathway preceded generalist sequestration of phenolics produced by multiple chemical pathways. We conclude that phenolics are consistently and selectively sequestered within Lithosiini. Furthermore, sequestration of compounds from a single chemical pathway may represent a synapomorphy of the tribe, and the ability to sequester phenolics produced by multiple pathways arose later. These findings expand on our understanding of the interactions between Lepidoptera and their lichen hosts.

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 α-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.