Low host-pathogen specificity in the leaf-cutting ant-microbe symbiosis

Abstract

Host-parasite associations are shaped by coevolutionary dynamics. One example is the complex fungus-growing ant-microbe symbiosis, which includes ancient host-parasite coevolution. Fungus-growing ants and the fungi they cultivate for food have an antagonistic symbiosis with Escovopsis, a specialized microfungus that infects the ants' fungus gardens. The evolutionary histories of the ant, cultivar and Escovopsis are highly congruent at the deepest phylogenetic levels, with specific parasite lineages exclusively associating with corresponding groups of ants and cultivar. Here, we examine host-parasite specificity at finer phylogenetic levels, within the most derived clade of fungus-growing ants, the leaf-cutters (Atta spp. and Acromyrmex spp.). Our molecular phylogeny of Escovopsis isolates from the leaf-cutter ant-microbe symbiosis confirms specificity at the broad phylogenetic level, but reveals frequent host-switching events between species and genera of leaf-cutter ants. Escovopsis strains isolated from Acromyrmex and Atta gardens occur together in the same clades, and very closely related strains can even infect the gardens of both ant genera. Experimental evidence supports low host-parasite specificity, with phylogenetically diverse strains of Escovopsis being capable of overgrowing all leaf-cutter cultivars examined. Thus, our findings indicate that this host-pathogen association is shaped by the farming ants having to protect their cultivated fungus from phylogenetically diverse Escovopsis garden pathogens.

Figure 1

Experimental setup of bioassay challenges between the fungus garden parasite Escovopsis and fungus garden pieces. (a) A garden piece freshly inoculated with Escovopsis (the parasite is indicated by an arrow). (b) An overgrown garden piece 5 days after infection; the garden piece is shrivelled and discoloured, and the parasite, which is growing on the garden piece, has sporulated (210×99 mm (600×600 DPI)).

Figure 2

Phylogenetic tree of 34 Escovopsis strains from leaf-cutting ant gardens and four outgroup strains of Escovopsis from Trachymyrmex gardens. Each parasite strain is indicated by the species name of the ant host garden from which Escovopsis was isolated. Upper node values correspond to maximum parsimony bootstrap proportions (only values greater than 90 are shown), while lower node values correspond to Bayesian PP (only values greater than 0.95 are shown). Branch colours correspond to two distinct Escovopsis clades (green, clade A; orange, clade B). The countries from which each strain was isolated are indicated by coloured abbreviations (PA, Panama; AR, Argentina; EC, Ecuador; MX, Mexico; GU, Guadeloupe; BR, Brazil; TR, Trinidad), followed by province or state names when available. Numbers in parentheses indicate strains that were used for bioassay challenges (table 2). ^* indicates a strain from an A. coronatus nest collected in Ecuador, colony code AGH030518-14; ^** indicates a strain from an A. echinatior nest collected in Panama, colony code CC020610-02 (§3).