Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants

Abstract

To combat disease, most fungus-growing ants (Attini) use antibiotics from mutualistic bacteria (Pseudonocardia) that are cultured on the ants' exoskeletons and chemical cocktails from exocrine glands, especially the metapleural glands (MG). Previous work has hypothesized that (i) Pseudonocardia antibiotics are narrow-spectrum and control a fungus (Escovopsis) that parasitizes the ants' fungal symbiont, and (ii) MG secretions have broad-spectrum activity and protect ants and brood. We assessed the relative importance of these lines of defence, and their activity spectra, by scoring abundance of visible Pseudonocardia for nine species from five genera and measuring rates of MG grooming after challenging ants with disease agents of differing virulence. Atta and Sericomyrmex have lost or greatly reduced the abundance of visible bacteria. When challenged with diverse disease agents, including Escovopsis, they significantly increased MG grooming rates and expanded the range of targets. By contrast, species of Acromyrmex and Trachymyrmex maintain abundant Pseudonocardia. When challenged, these species had lower MG grooming rates, targeted primarily to brood. More elaborate MG defences and reduced reliance on mutualistic Pseudonocardia are correlated with larger colony size among attine genera, raising questions about the efficacy of managing disease in large societies with chemical cocktails versus bacterial antimicrobial metabolites.

Generalized antifungal activity and 454-screening ofPseudonocardiaandAmycolatopsisbacteria in nests of fungus-growing ants

“…An integumental bacterial coat might protect the ants against bacterial or fungal infections to which the ants are exposed during their continuous shoulder rubbing with the microbial biofilms in their gardens. If so, the pseudonocardiaceous accretions on the integument may then complement or enhance the general antimicrobial role of metapleural gland secretions for protection of ants (41). This hypothesis could also explain why garden workers need and actually show higher Pseudonocardia loads than foragers (18,37).…”

“…Future studies should determine how many of these coexisting microbial lineages compete in situ (and thus could evolve competitive traits that harm the ants) and how many of them may complement each other's function as potential mutualists of the ants. (iv) Because pseudonocardiaceous secretions can severely harm the lepiotaceous cultivars, any application of secretion would have to be local [e.g., targeting critically diseased garden parts (41)] and the ants should prevent the spread of secretions across the garden at large. Rather than garden hygiene, possible alternate mutualistic roles of integumental microbes could include protection of the ants (Fig.…”

Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants

“…play an essential role (11,16) in the environment of leaf-cutting ants. The high variability in the quantities of valinomycin (3) in the waste of A. niger provides molecular proof that the antibiotics of the microbial symbionts of leaf-cutting ants can be highly localized (46). Therefore, it seems possible that the production of antibiotics may be regulated by the producing microorganisms or even the leaf-cutting ants (46).…”

Social insect genomes exhibit dramatic evolution in gene composition and regulation while preserving regulatory features linked to sociality

“…This pattern of rapid but transient expansions of gene content may coincide with dramatic life-history changes associated with early stages of lineage divergence. For example, A. cephalotes is distinguished from A. echinatior by loss of cuticular actinomycete cultures, physically distinct soldier castes, and claustral colony founding (Fernández-Marín et al 2009;Villesen et al 2009). In support of this, most leaf-cutter TRGs (68%) are species specific.…”