Dynamic Disease Management inTrachymyrmexFungus-Growing Ants (Attini: Formicidae)

Abstract

Multipartner mutualisms have potentially complex dynamics, with compensatory responses when one partner is lost or relegated to a minor role. Fungus-growing ants (Attini) are mutualistic associates of basidiomycete fungi and antibiotic-producing actinomycete bacteria; the former are attacked by specialized fungi (Escovopsis) and diverse generalist microbes. Ants deploy biochemical defenses from bacteria and metapleural glands (MGs) and express different behaviors to control contaminants. We studied four Trachymyrmex species that differed in relative abundance of actinomycetes to understand interactions among antimicrobial tactics that are contingent on the nature of infection. MG grooming rate and actinomycete abundance were negatively correlated. The two species with high MG grooming rates or abundant actinomycetes made relatively little use of behavioral defenses. Conversely, the two species with relatively modest biochemical defenses relied heavily on behavior. Trade-offs suggest that related species can evolutionarily diverge to rely on different defense mechanisms against the same threat. Neither bacterial symbionts nor MG secretions thus appear to be essential for mounting defenses against the specialized pathogen Escovopsis, but reduced investment in one of these defense modes tends to increase investment in the other.

Functional role of phenylacetic acid from metapleural gland secretions in controlling fungal pathogens in evolutionarily derived leaf-cutting ants

“…Two studies have now shown that MG compounds and secretions from Acromyrmex species can reduce mycelial growth or inhibit germination of Escovopsis conidia [29,30], but Acromyrmex workers only occasionally target Escovopsis infections behaviourally with their MG secretions [14], consistent with their actinomycetes being the main control strategy [14,45]. Our in vitro assays further showed that the PAA concentrations required to control Escovopsis were lower than those needed to control other pathogens, consistent with the hypothesis that these MG secretions, and PAA in particular, are alternative functional defences that have replaced actinomycete-bacteria-produced antibiotics used by Acromyrmex and most sympatric Trachymyrmex to control Escovopsis [14,15,28].…”

“…R. Soc. B 282: 20150212 lives up to common-sense sustainability criteria [14,15]. The main active control component PAA appears to be dynamically transferred from the MGs to the forelegs of workers to infection targets of both insect and fungus garden pathogens, after which a series of other grooming behaviours ensures that infective particles accumulate in the infrabuccal pockets of (particularly small and medium size) workers, where they are killed prior to permanent removal from the nest.…”

“…The treatments involved single inoculations with dry conidia from the insect pathogens Beauveria bassiana or Metarhizium brunneum, or from one of two strains of Escovopsis isolated from fungus gardens of A. cephalotes. Each experimental subcolony was inoculated with ca 1.5 Â 10 6 dry conidia [14,15], and controls were sham-inoculated by rubbing a sterile piece of paper on the fungus garden. Subcolonies were observed for 60 min after inoculation, and the frequency of each prophylactic behaviour recorded.…”

“…opportunities to understand how disease management strategies covary with social complexity [13][14][15].…”

“…Attine taxa differ in their reliance on bacteria-produced or glandular antimicrobials: species (or genera) with visible cuticular actinomycetes appear to apply MG secretions primarily to protect brood, while MG secretions are used more generally against fungus garden, brood and adult infections in ants that lack these bacteria [14,15]. The significance of MG-secretion use in disease control has largely been inferred from behavioural observations of MG grooming, combined with correlative data on pathogen growth inhibition ( [14,15], but see [27][28][29]). The transfer of MG secretions to infected tissues has not been confirmed by target-specific chemical assays, and few studies have tested the efficacy of particular compounds as antibiotics [30].…”