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1. The Last Piece of the Puzzle? Phylogenetic Position and Natural History of the Monotypic Fungus-Farming Ant Genus Paramycetophylax (Formicidae: Attini)

   https://doi.org/10.1093/isd/ixab029  

   Hanisch, Priscila Elena; Sosa-Calvo, Jeffrey; Schultz, Ted R (January 2022, Insect Systematics and Diversity)

   Camacho, Gabriela P (Ed.)

   Abstract The evolutionary history of fungus-farming ants has been the subject of multiple morphological, molecular phylogenetic, and phylogenomic studies. Due to its rarity, however, the phylogenetic position, natural history, and fungal associations of the monotypic genus Paramycetophylax Kusnezov have remained enigmatic. Here we report the first excavations of colonies of Paramycetophylax bruchi (Santschi) and describe its nest architecture and natural history. Utilizing specimens from these collections, we generated ultraconserved-element (UCE) data to determine the evolutionary position of Paramycetophylax within the fungus-farming ants and ribosomal ‘fungal barcoding’ ITS sequence data to identify the fungal cultivar. A maximum-likelihood phylogenomic analysis indicates that the genus Paramycetophylax is the sister group of the yeast-cultivating Cyphomyrmex rimosus group, an unexpected result that renders the genus Cyphomyrmex Mayr paraphyletic. A Bayesian divergence-dating analysis indicates that Paramycetophylax diverged from its sister group around 36 mya (30–42 mya, HPD) in the late Eocene-early Oligocene, a period of global cooling, expansion of grasslands, and large-scale extinction of tropical organisms. Bayesian analysis of the fungal cultivar ITS gene fragment indicates that P. bruchi practices lower agriculture and that the cultivar grown by P. bruchi belongs to the Clade 1 group of lower-attine fungi, a clade that, interestingly, also includes the C. rimosus-group yeast cultivars. Based on these results, we conclude that a better understanding of P. bruchi and its fungal cultivar, including whole-genome data, is critical for reconstructing the origin of yeast agriculture, a major transition in the evolution of fungus-farming ants. 

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2. Genomic diversification of the specialized parasite of the fungus-growing ant symbiosis

   https://doi.org/10.1073/pnas.2213096119  

   Gotting, Kirsten; May, Daniel S.; Sosa-Calvo, Jeffrey; Khadempour, Lily; Francoeur, Charlotte B.; Berasategui, Aileen; Thairu, Margaret W.; Sandstrom, Shelby; Carlson, Caitlin M.; Chevrette, Marc G.; et al (December 2022, Proceedings of the National Academy of Sciences)

   Fungi shape the diversity of life. Characterizing the evolution of fungi is critical to understanding symbiotic associations across kingdoms. In this study, we investigate the genomic and metabolomic diversity of the genus Escovopsis , a specialized parasite of fungus-growing ant gardens. Based on 25 high-quality draft genomes, we show that Escovopsis forms a monophyletic group arising from a mycoparasitic fungal ancestor 61.82 million years ago (Mya). Across the evolutionary history of fungus-growing ants, the dates of origin of most clades of Escovopsis correspond to the dates of origin of the fungus-growing ants whose gardens they parasitize. We reveal that genome reduction, determined by both genomic sequencing and flow cytometry, is a consistent feature across the genus Escovopsis, largely occurring in coding regions, specifically in the form of gene loss and reductions in copy numbers of genes. All functional gene categories have reduced copy numbers, but resistance and virulence genes maintain functional diversity. Biosynthetic gene clusters (BGCs) contribute to phylogenetic differences among Escovopsis spp., and sister taxa in the Hypocreaceae. The phylogenetic patterns of co-diversification among BGCs are similarly exhibited across mass spectrometry analyses of the metabolomes of Escovopsis and their sister taxa. Taken together, our results indicate that Escovopsis spp. evolved unique genomic repertoires to specialize on the fungus-growing ant-microbe symbiosis. 

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3. 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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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. The Convergent Evolution of Agriculture in Humans and Insects

   https://doi.org/10.7551/mitpress/13600.001.0001  

   Schultz, Ted R; Gawne, Richard; Peregrine, Peter N (February 2022, The MIT Press)

   Schultz, Ted R; Gawne, Richard; Peregrine, Peter N (Ed.)

   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 

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