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 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.
Centro de Biodiversidad y Descubrimiento de Drogas, Instituto de Investigaciones Científicas y Servicios de Alta Tecnología, Edificio 219, Ciudad del Saber, Clayton, Panamá Centre for Social Evolution, Department of Biology, University of Copenhagen Universitetsparken 15, Copenhagen 2100, Denmark Smithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, Ancón, Republic of Panamá hfernandez@indicasat.org.pa.
Hermógenes
http://orcid.org/0000-0001-7200-384X
H
Fernández-Marín
Centre for Social Evolution, Department of Biology, University of Copenhagen Universitetsparken 15, Copenhagen 2100, Denmark.
David R
DR
Nash
Smithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, Ancón, Republic of Panamá
Sarah
S
Higginbotham
Smithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, Ancón, Republic of Panamá
Catalina
C
Estrada
Centre for Social Evolution, Department of Biology, University of Copenhagen Universitetsparken 15, Copenhagen 2100, Denmark Laboratory of Socioecology and Social Evolution, Zoological Institute, University of Leuven, Naamsestraat 59, box 2466, Leuven 3000, Belgium.
Jelle S
JS
van Zweden
Centre for Social Evolution, Department of Biology, University of Copenhagen Universitetsparken 15, Copenhagen 2100, Denmark Laboratoire d'Ethologie Expérimentale et Comparée (LEEC), University of Paris 13, Sorbonne Paris Cité, France.
Patrizia
P
d'Ettorre
Smithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, Ancón, Republic of Panamá
William T
WT
Wcislo
Centre for Social Evolution, Department of Biology, University of Copenhagen Universitetsparken 15, Copenhagen 2100, Denmark jjboomsma@bio.ku.dk.
Jacobus J
JJ
Boomsma
D000818:Animals; D001000:Ants / Q000378:metabolism* / Q000382:microbiology; D005075:Biological Evolution; D005088:Exocrine Glands / Q000378:metabolism*; D006999:Hypocreales / Q000502:physiology*; D052981:Metarhizium / Q000502:physiology*; D010648:Phenylacetates / Q000378:metabolism*; D013045:Species Specificity
D010648:Phenylacetates; C025136:phenylacetic acid
Attini; Escovopsis; actinomycetes; entomopathogens; mutualism; symbiosis