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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. 

The ability to recognize nestmates is critical to the ecological success of social insects. Fungus-farming “attine” ants (Formicidae: Myrmicinae: Attini: Attina) can recognize their nestmates and symbiotic fungi via chemoreception. Although it has been shown that mutualistic fungi release volatile compounds that elicit responses in fungus-farming ants, the compounds and the sensory mechanisms involved remain little studied. Here, we characterize compounds found in attine fungus gardens and explore the correlations between those compounds, fungal substrates, and the laboratory environment. We also characterize ant cuticular hydrocarbons from Atta cephalotes colonies of the same species maintained in the same laboratory conditions for two or more years. Using gas chromatography associated with mass spectrometry, we verified that both substrate (i.e., the food on which fungus gardens grow) and environmental origin may influence the volatiles the fungus releases. We found compounds related to the environment, including naphthalene. We show that the volatile profiles of fungal strains grown by Atta cephalotes are most similar to each other, whereas the profile of the fungus grown by ants in the genus Cyphomyrmex is more similar to that of their substrate than to the profiles of other cultivated fungi. Regarding cuticular hydrocarbons, we found that ants collected in the same location have more similar hydrocarbon profiles than ants of the same species collected in a different location, even if all the colonies had been maintained under the same conditions (temperature, substrate) for extended periods. Our results provide strong evidence that a combination of species genetics and environmental factors shape variations in the volatile chemical profiles of cultivated fungi. After long homogenization, ants still demonstrate a solid difference among the cuticular profiles. 

Abstract The classification of ants (Hymenoptera: Formicidae) has progressed in waves since the first 17 species were described by Linnaeus in the 1758 edition of Systema Naturae. Since then, over 18,000 species-rank names have accumulated for the global myrmecofauna, of which ~14,260 living and ~810 fossil species are valid. Here, we provide a synopsis of ant biodiversity and review the history and classification of the family, while highlighting the massive growth of the field in the new millennium. We observe that major transformation has occurred for ant classification due to advances in DNA sequencing technologies, model-based hypothesis testing, and imaging technologies. We therefore provide a revised and illustrated list of diagnostic character states for the higher clades of Formicidae, recognizing that vastly more work is to be done. To facilitate discussion and the systematic accumulation of evolutionary knowledge for the early evolution of the ants, we suggest an informal nomenclatural system for the higher clades of ants, based on names currently in use and a set of names that have been democratically selected by the authors. To guide future work on ant systematics, we summarize currently available databases and present perspectives on regions in need of biodiversity exploration, challenges facing the field, and the future of ant taxonomy. 

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. 

Contributors explore common elements in the evolutionary histories of both human and insect agriculture resulting from convergent evolution. During the past 12,000 years, agriculture originated in humans as many as twenty-three times, and during the past 65 million years, agriculture also originated in nonhuman animals at least twenty times and in insects at least fifteen times. It is much more likely that these independent origins represent similar solutions to the challenge of growing food than that they are due purely to chance. This volume seeks to identify common elements in the evolutionary histories of both human and insect agriculture that are the results of convergent evolution. The goal is to create a new, synthetic field that characterizes, quantifies, and empirically documents the evolutionary and ecological mechanisms that drive both human and nonhuman agriculture. The contributors report on the results of quantitative analyses comparing human and nonhuman agriculture; discuss evolutionary conflicts of interest between and among farmers and cultivars and how they interfere with efficiencies of agricultural symbiosis; describe in detail agriculture in termites, ambrosia beetles, and ants; and consider patterns of evolutionary convergence in different aspects of agriculture, comparing fungal parasites of ant agriculture with fungal parasites of human agriculture, analyzing the effects of agriculture on human anatomy, and tracing the similarities and differences between the evolution of agriculture in humans and in a single, relatively well-studied insect group, fungus-farming ants. Contributors Duur K. Aanen, Niels P. R. Anten, Peter H. W. Biedermann, Jacobus J. Boomsma, Laura T. Buck, Guillaume Chomicki, Tim Denham, R. Ford Denison, Dorian Q. Fuller, Richard Gawne, Nicole M. Gerardo, Thomas C. Harrington, Ana Ješovnik, Judith Korb, Chase G. Mayers, George R. McGhee, Kenneth Z. McKenna, Lumila P. Menéndez, Peter N. Peregrine, Ted R. Schultz