TY - JOUR

T1 - Functional role of phenylacetic acid from metapleural gland secretions in controlling fungal pathogens in evolutionarily derived leaf-cutting ants

AU - Fernández-Marín, Hermógenes

AU - Nash, David Richard

AU - Higginbotham, Sarah

AU - Estrada, Catalina

AU - van Zweden, Jelle Stijn

AU - D'Ettorre, Patrizia

AU - Wcislo, William T.

AU - Boomsma, Jacobus Jan

PY - 2015

Y1 - 2015

N2 - Fungus-farming ant colonies vary four to five orders of magnitude in size. Theyemploy compounds from actinomycete bacteria and exocrine glands as antimicrobialagents. Atta colonies have millions of ants and are particularlyrelevant for understanding hygienic strategies as they have abandoned theirancestors’ prime dependence on antibiotic-based biological control in favourof using metapleural gland (MG) chemical secretions. Atta MGs are unique insynthesizing large quantities of phenylacetic acid (PAA), a known but littleinvestigated antimicrobial agent.We showthat particularly the smallestworkersgreatly reduce germination rates of Escovopsis and Metarhizium spores afteractively applying PAA to experimental infection targets in garden fragmentsandtransferring the spores to the ants’ infrabuccal cavities. In vitro assays furtherindicated that Escovopsis strains isolated fromevolutionarily derived leaf-cuttingants are less sensitive to PAA than strains from phylogenetically more basalfungus-farming ants, consistent with the dynamics of an evolutionary armsrace between virulence and control for Escovopsis, but not Metarhizium. Attaants form larger colonies with more extreme caste differentiation relative toother attines, in societies characterized by an almost complete absence of reproductiveconflicts.We hypothesize that these changes are associatedwith uniqueevolutionary innovations in chemical pest management that appear robustagainst selection pressure for resistance by specialized mycopathogens.

AB - Fungus-farming ant colonies vary four to five orders of magnitude in size. Theyemploy compounds from actinomycete bacteria and exocrine glands as antimicrobialagents. Atta colonies have millions of ants and are particularlyrelevant for understanding hygienic strategies as they have abandoned theirancestors’ prime dependence on antibiotic-based biological control in favourof using metapleural gland (MG) chemical secretions. Atta MGs are unique insynthesizing large quantities of phenylacetic acid (PAA), a known but littleinvestigated antimicrobial agent.We showthat particularly the smallestworkersgreatly reduce germination rates of Escovopsis and Metarhizium spores afteractively applying PAA to experimental infection targets in garden fragmentsandtransferring the spores to the ants’ infrabuccal cavities. In vitro assays furtherindicated that Escovopsis strains isolated fromevolutionarily derived leaf-cuttingants are less sensitive to PAA than strains from phylogenetically more basalfungus-farming ants, consistent with the dynamics of an evolutionary armsrace between virulence and control for Escovopsis, but not Metarhizium. Attaants form larger colonies with more extreme caste differentiation relative toother attines, in societies characterized by an almost complete absence of reproductiveconflicts.We hypothesize that these changes are associatedwith uniqueevolutionary innovations in chemical pest management that appear robustagainst selection pressure for resistance by specialized mycopathogens.

KW - mutualism

KW - symbiosis

KW - Attini

KW - Escovopsis

KW - actinomycetes

KW - entomopathogens

U2 - 10.1098/rspb.2015.0212

DO - 10.1098/rspb.2015.0212

M3 - Journal article

C2 - 25925100

VL - 282

JO - Proceedings of the Royal Society B: Biological Sciences

JF - Proceedings of the Royal Society B: Biological Sciences

SN - 0962-8452

IS - 1807

ER -