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1. Laboratory Environment Affects the Volatiles of Fungus Gardens in the Colonies of Fungus-farming Ants

   https://doi.org/10.13102/sociobiology.v72i1.9768  

   Assis, Diego Santana; Schultz, Ted; Brodowski, Skylar; Newsome, Gabriel Asher; Nascimento, Fabio_Santos do (January 2025, Sociobiology)

   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. 

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2. The coevolution of fungus-ant agriculture

   https://doi.org/10.1126/science.adn7179  

   Schultz, Ted R; Sosa-Calvo, Jeffrey; Kweskin, Matthew P; Lloyd, Michael W; Dentinger, Bryn; Kooij, Pepijn W; Vellinga, Else C; Rehner, Stephen A; Rodrigues, Andre; Montoya, Quimi V; et al (October 2024, Science)

   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. 

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3. Fungus-Farming Ants (Attini in Part)

   https://doi.org/10.1007/978-3-319-90306-4_46-1  

   Schultz, Ted R (December 2019, Springer International Publishing)
4. Burkholderia from Fungus Gardens of Fungus-Growing Ants Produces Antifungals That Inhibit the Specialized Parasite Escovopsis

   https://doi.org/10.1128/AEM.00178-21  

   Francoeur, Charlotte B.; May, Daniel S.; Thairu, Margaret W.; Hoang, Don Q.; Panthofer, Olivia; Bugni, Tim S.; Pupo, Mônica T.; Clardy, Jon; Pinto-Tomás, Adrián A.; Currie, Cameron R. (June 2021, Applied and Environmental Microbiology)

   Rudi, Knut (Ed.)

   ABSTRACT Within animal-associated microbiomes, the functional roles of specific microbial taxa are often uncharacterized. Here, we use the fungus-growing ant system, a model for microbial symbiosis, to determine the potential defensive roles of key bacterial taxa present in the ants’ fungus gardens. Fungus gardens serve as an external digestive system for the ants, with mutualistic fungi in the genus Leucoagaricus converting the plant substrate into energy for the ants. The fungus garden is host to specialized parasitic fungi in the genus Escovopsis . Here, we examine the potential role of Burkholderia spp. that occur within ant fungus gardens in inhibiting Escovopsis. We isolated members of the bacterial genera Burkholderia and Paraburkholderia from 50% of the 52 colonies sampled, indicating that members of the family Burkholderiaceae are common inhabitants in the fungus gardens of a diverse range of fungus-growing ant genera. Using antimicrobial inhibition bioassays, we found that 28 out of 32 isolates inhibited at least one Escovopsis strain with a zone of inhibition greater than 1 cm. Genomic assessment of fungus garden-associated Burkholderiaceae indicated that isolates with strong inhibition all belonged to the genus Burkholderia and contained biosynthetic gene clusters that encoded the production of two antifungals: burkholdine1213 and pyrrolnitrin. Organic extracts of cultured isolates confirmed that these compounds are responsible for antifungal activities that inhibit Escovopsis but, at equivalent concentrations, not Leucoagaricus spp. Overall, these new findings, combined with previous evidence, suggest that members of the fungus garden microbiome play an important role in maintaining the health and function of fungus-growing ant colonies. IMPORTANCE Many organisms partner with microbes to defend themselves against parasites and pathogens. Fungus-growing ants must protect Leucoagaricus spp., the fungal mutualist that provides sustenance for the ants, from a specialized fungal parasite, Escovopsis . The ants take multiple approaches, including weeding their fungus gardens to remove Escovopsis spores, as well as harboring Pseudonocardia spp., bacteria that produce antifungals that inhibit Escovopsis. In addition, a genus of bacteria commonly found in fungus gardens, Burkholderia , is known to produce secondary metabolites that inhibit Escovopsis spp. In this study, we isolated Burkholderia spp. from fungus-growing ants, assessed the isolates’ ability to inhibit Escovopsis spp., and identified two compounds responsible for inhibition. Our findings suggest that Burkholderia spp. are often found in fungus gardens, adding another possible mechanism within the fungus-growing ant system to suppress the growth of the specialized parasite Escovopsis . 

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5. Why is the world's most expensive fungus disappearing?

   Hopping, Kelly A.; Chignell, Stephen M.; Lambin, Eric F. (January 2019, Environmental science journal for teens)

   Meet the world’s most wanted parasite: a mummified caterpillar with a fungus growing right out of its face. Even stranger: it costs three times its weight in gold! This super expensive fungus grows in the alpine regions of the Himalayas and Tibetan Plateau where it is cold and dry. Its promised health benefits include increased strength and cures for many diseases. Recently, it has become very popular around the world. Its price has increased and collectors have started harvesting more. But lately, some people have become concerned that the fungus populations are declining. We wanted to see if that is the case, and if so, why? So, we interviewed local harvesters and analyzed environmental models of the region. Our results showed that there is a decline in the caterpillar fungus populations, and the main causes are overharvesting and climate change. 

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