An Old World leaf‐cutting, fungus‐growing ant: A case of convergent evolution

Abstract

The African myrmicine ant Crematogaster clariventris is a territorially dominant arboreal species that constructs very hard carton nests. Noting that workers cut off leaves from different plant species while building or repairing their nests, we asked ourselves if there was a correlation. We conducted scanning electron microscopic observations of nest walls that revealed the presence of fungal mycelia. As the presence of filamentous Ascomycota has been shown on arboreal ant nests worldwide, we used a metabarcoding approach and, indeed, noted the presence of Operational Taxonomic Unit (OTU) Cre_006041 of the Capnodiales known to reinforce large nests of an unidentified African Crematogaster. This OTU was also recorded in the workers' bodies.At a very low level, we also noted OTU Cre_320021 of the Chaetothyriales known for their relationships with the African plant-ant species C. margaritae. Therefore, by cutting leaves and growing fungus, C. clariventris illustrates a case of convergent evolution with higher New World leaf-cutting, fungus-growing Attina of the genera Acromyrmex, Amoimyrmex and Atta. However, there are notable differences. Leafcutting Attina cultivate Agaricaceae (Basidiomycota) for food, whereas C. clariventris uses Capnodiales to reinforce their nests (i.e., after the mycelium died, the hyphae's cell walls remained sturdy forming a natural composite material), have a distinct geographical origin (i.e., New World vs. Old World) and belong to a distinct ant tribe in the subfamily Myrmicinae (i.e., Attini vs. Crematogastrini). Furthermore, leaf-cutting Attina evolved an efficacious means of cutting leaves by using their mandibles asymmetrically, whereas C. clariventris workers, typically, use their mandibles symmetrically.

Fungi as mutualistic partners in ant-plant interactions

“…Ant-associated fungi of Functional Group I are exposed to the environment and must be able to withstand extreme conditions like heavy rain, high temperatures, desiccation, intense solar radiation, nutrient scarcity, and a constant exposure to fungal competitors. Chaetothyriales (Ascomycota, Eurotiomycetes) and Capnodiales (including Mycosphaerellales) (Ascomycota, Dothideomycetes) were frequently isolated from hyphal fragments of nest walls, galleries, and carton structures, as were Venturiaceae (Ascomycota, Dothideomycetes, Pleosporales) in rare cases ( Mayer and Voglmayr, 2009 ; Voglmayr et al., 2011 ; Seipke et al., 2012 ; Nepel et al., 2014 ; Dejean et al., 2023 ). Strains that occur in this environment have highly melanized cell walls ( Figures 1B-E, G, K, L ) as melanization is enabling fungi to tolerate physical stress ( Cordero and Casadevall, 2017 ).…”

Mutualistic interactions between ants and fungi: A review

“…Indeed, there is a fundamental difference with leaf‐cutting Attina that cultivate Basidiomycota for food (the mycelium is kept alive), whereas Cr. clariventris workers grow fungi of the orders Capnodiales and likely Chaetothyriales to reinforce the carton of their nests (Dejean et al, 2023 ; Schultz, 2021 ; Figure 1 ). Because the mutualism is based on the death of the mycelium, there is a specific case of fungal agriculture for Cr.…”