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Symbiotic relationships shape the evolution of organisms. Fungi in the genus Escovopsis share an evolutionary history with the fungus-growing “attine” ant system and are only found in association with these social insects. Despite this close relationship, there are key aspects of Escovopsis evolution that remain poorly understood. To gain further insight into the evolutionary history of these unique fungi, we delve deeper into Escovopsis’ origin and distribution, considering the largest sampling, so far, across the Americas. Furthermore, we investigate Escovopsis’ trait evolution, and relationship with attine ants. We demonstrate that, while the genus originated approximately 56.9 Mya, it only became associated with 'higher attine' ants in the last 38 My. Our results, however, indicate that it is likely that the ancestor of Escovopsis lived in symbiosis with early-diverging fungus-growing ants. Since then, the fungi have evolved morphological and physiological adaptations that have increased their reproductive efficiency, possibly to overcome barriers mounted by the ants and their other associated microbes. Taken together, these results provide new clues as to how Escovopsis has evolved within the context of this complex symbiosis and shed light on the evolutionary history of the fungus-growing ant system. 

Abstract Diet profoundly influences the composition of an animal’s microbiome, especially in holometabolous insects, offering a valuable model to explore the impact of diet on gut microbiome dynamics throughout metamorphosis. Here, we use monarch butterflies (Danaus plexippus), specialist herbivores that feed as larvae on many species of chemically well-defined milkweed plants (Asclepias sp.), to investigate the impacts of development and diet on the composition of the gut microbial community. While a few microbial taxa are conserved across life stages of monarchs, the microbiome appears to be highly dynamic throughout the life cycle. Microbial diversity gradually diminishes throughout the larval instars, ultimately reaching its lowest point during the pupal stage and then recovering again in the adult stage. The microbial composition then undergoes a substantial shift upon the transition from pupa to adult, with female adults having significantly different microbial communities than the eggs that they lay, indicating limited evidence for vertical transmission of gut microbiota. While diet did not significantly impact overall microbial composition, our results suggest that fourth instar larvae exhibit higher microbial diversity when consuming milkweed with high concentrations of toxic cardenolide phytochemicals. This study underscores how diet and developmental stage collectively shape the monarch’s gut microbiota. 

Fungus-farming ants cultivate multiple lineages of fungi for food, but, because fungal cultivar relationships are largely unresolved, the history of fungus-ant coevolution remains poorly known. We designed probes targeting >2000 gene regions to generate a dated evolutionary tree for 475 fungi and combined it with a similarly generated tree for 276 ants. We found that fungus-ant agriculture originated ~66 million years ago when the end-of-Cretaceous asteroid impact temporarily interrupted photosynthesis, causing global mass extinctions but favoring the proliferation of fungi. Subsequently, ~27 million years ago, one ancestral fungal cultivar population became domesticated, i.e., obligately mutualistic, when seasonally dry habitats expanded in South America, likely isolating the cultivar population from its free-living, wet forest–dwelling conspecifics. By revealing these and other major transitions in fungus-ant coevolution, our results clarify the historical processes that shaped a model system for nonhuman agriculture. 

Abstract Escovopsis is a diverse group of fungi, which are considered specialized parasites of the fungal cultivars of fungus-growing ants. The lack of a suitable taxonomic framework and phylogenetic inconsistencies have long hampered Escovopsis research. The aim of this study is to reassess the genus Escovopsis using a taxonomic approach and a comprehensive multilocus phylogenetic analysis, in order to set the basis of the genus systematics and the stage for future Escovopsis research. Our results support the separation of Escovopsis into three distinct genera. In light of this, we redefine Escovopsis as a monophyletic clade whose main feature is to form terminal vesicles on conidiophores. Consequently, E. kreiselii and E. trichodermoides were recombined into two new genera, Sympodiorosea and Luteomyces , as S . kreiselii and L . trichodermoides , respectively. This study expands our understanding of the systematics of Escovopsis and related genera, thereby facilitating future research on the evolutionary history, taxonomic diversity, and ecological roles of these inhabitants of the attine ant colonies. 

Fungi in the genus Escovopsis (Ascomycota: Hypocreales) are prevalent associates of the complex symbiosis between fungus-growing ants (Tribe Attini), the ants’ cultivated basidiomycete fungi and a consortium of both beneficial and harmful microbes found within the ants’ garden communities. Some Escovopsis spp. have been shown to attack the ants’ cultivated fungi, and co-infections by multiple Escovopsis spp. are common in gardens in nature. Yet, little is known about how Escovopsis strains impact each other. Since microbe–microbe interactions play a central role in microbial ecology and evolution, we conducted experiments to assay the types of interactions that govern Escovopsis–Escovopsis relationships. We isolated Escovopsis strains from the gardens of 10 attine ant genera representing basal (lower) and derived groups in the attine ant phylogeny. We conducted in vitro experiments to determine the outcome of both intraclonal and interclonal Escovopsis confrontations. When paired with self (intraclonal interactions), Escovopsis isolated from lower attine colonies exhibited antagonistic (inhibitory) responses, while strains isolated from derived attine colonies exhibited neutral or mutualistic interactions, leading to a clear phylogenetic pattern of interaction outcome. Interclonal interactions were more varied, exhibiting less phylogenetic signal. These results can serve as the basis for future studies on the costs and benefits of Escovopsis coinfection, and on the genetic and chemical mechanisms that regulate the compatibility and incompatibility observed here.