The agricultural pathology of ant fungus gardens.

Gardens of fungus-growing ants (Formicidae: Attini) traditionally have been thought to be free of microbial parasites, with the fungal mutualist maintained in nearly pure "monocultures." We conducted extensive isolations of "alien" (nonmutualistic) fungi from ant gardens of a phylogenetically representative collection of attine ants. Contrary to the long-standing assumption that gardens are maintained free of microbial pathogens and parasites, they are in fact host to specialized parasites that are only known from attine gardens and that are found in most attine nests. These specialized garden parasites, belonging to the microfungus genus Escovopsis (Ascomycota: anamorphic Hypocreales), are horizontally transmitted between colonies. Consistent with theory of virulence evolution under this mode of pathogen transmission, Escovopsis is highly virulent and has the potential for rapid devastation of ant gardens, leading to colony mortality. The specialized parasite Escovopsis is more prevalent in gardens of the more derived ant lineages than in gardens of the more "primitive" (basal) ant lineages. Because fungal cultivars of derived attine lineages are asexual clones of apparently ancient origin whereas cultivars of primitive ant lineages were domesticated relatively recently from free-living sexual stocks, the increased virulence of pathogens associated with ancient asexual cultivars suggests an evolutionary cost to cultivar clonality, perhaps resulting from slower evolutionary rates of cultivars in the coevolutionary race with their pathogens.

[1]  T. D. Lucia,et al.  Escovopsis, a new genus from leaf cutting ant nests to replace Phialocladus nomem invalidum , 1990 .

[2]  A. Hervey,et al.  Antibiotic metabolite of a fungus cultivated by gardening ants. , 1979, Mycologia.

[3]  G. B. Lucas.  The War Against Blue Mold , 1980, Science.

[4]  J. M. Cherrett,et al.  The role of leaf‐cutting ant workers (Hymenoptera: Formicidae) in fungus garden maintenance , 1994 .

[5]  W. M. Wheeler,et al.  Ants : their structure, development and behavior , 1960 .

[6]  Alfred Möller.  Die Pilzgärten einiger südamerikanischer Ameisen , 1893 .

[7]  T. Schultz,et al.  Acromyrmex insinuator new species: an incipient social parasite of fungus-growing ants , 1998, Insectes Sociaux.

[8]  G. E. Michaels,et al.  Attine Fungus Gardens Contain Yeasts , 1970, Science.

[9]  D. J. Stradling,et al.  Microfungi in the fungus gardens of the leaf-cutting ant Atta cephalotes: a preliminary study , 1996 .

[10]  W. Hamilton,et al.  Sex against virulence: the coevolution of parasitic diseases. , 1996, Trends in ecology & evolution.

[11]  J. Brown,et al.  Chance and selection in the evolution of barley mildew. , 1994, Trends in microbiology.

[12]  K. Seifert,et al.  Escovopsis aspergilloides, a rediscovered hyphomycete from leaf-cutting ant nests , 1995 .

[13]  T. Schultz,et al.  Phylogeny of fungus-growing ants (Tribe Attini) based on mtDNA sequence and morphology. , 1998, Molecular phylogenetics and evolution.

[14]  T. Schultz,et al.  A phylogenetic analysis of the fungus‐growing ants (Hymenoptera: Formicidae: Attini) based on morphological characters of the larvae , 1995 .

[15]  U. Mueller,et al.  The evolution of agriculture in ants , 1998, Science.

[16]  Michael Martin.  Invertebrate-Microbial Interactions , 2020 .

[17]  Ted R. Schultz,et al.  Evolutionary History of the Symbiosis Between Fungus-Growing Ants and Their Fungi , 1994, Science.

[18]  E. Wilson.  The Insect Societies , 1974 .

[19]  W. Hamilton.  Sex versus non-sex versus parasite , 1980 .

[20]  L. Cook,et al.  Genetic consequences of man made change , 1981 .

[21]  James A. Scott,et al.  Fungus-growing ants use antibiotic-producing bacteria to control garden parasites , 1999, Nature.

[22]  H. Schildknecht,et al.  Plant bioregulators in the metathoracic glands of myrmicine ants. , 1970, Angewandte Chemie.