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

Fungus-farming ant colonies vary four to five orders of magnitude in size. They employ compounds from actinomycete bacteria and exocrine glands as antimicrobial agents. Atta colonies have millions of ants and are particularly relevant for understanding hygienic strategies as they have abandoned thei...

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Published in:Proceedings of the Royal Society. B, Biological sciences Biological sciences, 2015-05, Vol.282 (1807), p.20150212-20150212
Main Authors: Fernández-Marín, Hermógenes, Nash, David R., Higginbotham, Sarah, Estrada, Catalina, van Zweden, Jelle S., d'Ettorre, Patrizia, Wcislo, William T., Boomsma, Jacobus J.
Format: Article
Language:English
Subjects:
Actinomycetes
Animals
Ants - metabolism
Ants - microbiology
Atta
Attini
Biological Evolution
Entomopathogens
Escovopsis
Exocrine Glands - secretion
Formicidae
Hypocreales - physiology
Metarhizium
Metarhizium - physiology
Mutualism
Phenylacetates - metabolism
Species Specificity
Symbiosis
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Summary:Fungus-farming ant colonies vary four to five orders of magnitude in size. They employ compounds from actinomycete bacteria and exocrine glands as antimicrobial agents. Atta colonies have millions of ants and are particularly relevant for understanding hygienic strategies as they have abandoned their ancestors' prime dependence on antibiotic-based biological control in favour of using metapleural gland (MG) chemical secretions. Atta MGs are unique in synthesizing large quantities of phenylacetic acid (PAA), a known but little investigated antimicrobial agent. We show that particularly the smallest workers greatly reduce germination rates of Escovopsis and Metarhizium spores after actively applying PAA to experimental infection targets in garden fragments and transferring the spores to the ants' infrabuccal cavities. In vitro assays further indicated that Escovopsis strains isolated from evolutionarily derived leaf-cutting ants are less sensitive to PAA than strains from phylogenetically more basal fungus-farming ants, consistent with the dynamics of an evolutionary arms race between virulence and control for Escovopsis, but not Metarhizium. Atta ants form larger colonies with more extreme caste differentiation relative to other attines, in societies characterized by an almost complete absence of reproductive conflicts. We hypothesize that these changes are associated with unique evolutionary innovations in chemical pest management that appear robust against selection pressure for resistance by specialized mycopathogens.
ISSN:0962-8452
1471-2954
DOI:10.1098/rspb.2015.0212