Reciprocal genomic evolution in the ant–fungus agricultural symbiosis

Abstract

The attine ant–fungus agricultural symbiosis evolved over tens of millions of years, producing complex societies with industrial-scale farming analogous to that of humans. Here we document reciprocal shifts in the genomes and transcriptomes of seven fungus-farming ant species and their fungal cultivars. We show that ant subsistence farming probably originated in the early Tertiary (55–60 MYA), followed by further transitions to the farming of fully domesticated cultivars and leaf-cutting, both arising earlier than previously estimated. Evolutionary modifications in the ants include unprecedented rates of genome-wide structural rearrangement, early loss of arginine biosynthesis and positive selection on chitinase pathways. Modifications of fungal cultivars include loss of a key ligninase domain, changes in chitin synthesis and a reduction in carbohydrate-degrading enzymes as the ants gradually transitioned to functional herbivory. In contrast to human farming, increasing dependence on a single cultivar lineage appears to have been essential to the origin of industrial-scale ant agriculture.

Lignocellulose pretreatment in a fungus-cultivating termite

“…the paradigm for wood decay, our findings add to the growing body of contention that ectosymbiotic fungi of fungus-cultivating insects (ants and termites) are likely to lose the key delignification potential throughout evolutionary modifications (45). In the funguscultivating termite symbiotic system, lignin depolymerization takes place during the rapid passage through the pH-neutral gut of young worker termites (46) in a process that is striking in its speed and efficiency at destroying the traditionally considered mostrecalcitrant C-C-bonded lignin structural units, thereby facilitating efficient degradation of the substrate by processes subsequently occurring via the fungus-comb microbiome.…”

Nutrition mediates the expression of cultivar–farmer conflict in a fungus-growing ant

“…This commitment to farming later led to the emergence of the "higher attines," including the Acromyrmex and Atta leafcutter ants that rear truly domesticated and coevolving cultivars on fresh plant-material substrates (22)(23)(24)(25). However, it has remained underappreciated that relatively unproductive farming in the lower attines has otherwise been very successful in coping with the nutritional challenges of an exclusive fungal diet, in maintaining homeostatic growth conditions for small gardens, and in controlling fungal pathogens and social parasites (26)(27)(28).…”

“…specialized in farming gardens of basidiomycete fungi provisioned with nutritionally poor forest-floor detritus (21)(22)(23). This commitment to farming later led to the emergence of the "higher attines," including the Acromyrmex and Atta leafcutter ants that rear truly domesticated and coevolving cultivars on fresh plant-material substrates (22)(23)(24)(25).…”

The interactions of ants with their biotic environment

“…the fire ant: Solenopsis invicta [110]; the Argentine ant: Linepithema humile [111]; the red harvester ant: Pogonomyrmex barbatus [112]; the leafcutter ant Atta cephalotes [113] and Pseudomyrmex plant ants [114]) and ever faster and low-cost, next-generation sequencing approaches and gene expression studies for targeted tissues and genes. Genomic approaches will allow a new understanding of ant biotic interactions by revealing discrete or genome-wide selection, gene duplication or loss or gene expression changes linked to new interactions [8,115]. Another emerging theme is multi-partite interactions, how they evolve and how the benefits are negotiated between species.…”