Gardens of fungus-growing ants (Formicidae: Attini) traditionally have been
thought to be free of microbial parasites with the fungal mutualist mainta
ined in nearly pure "monocultures." We conducted extensive isolations of "a
lien" (nonmutualistic) fungi from ant gardens of a phylogenetically represe
ntative collection of attine ants. Contrary to the long-standing assumption
that gardens are maintained free of microbial pathogens and parasites, the
y 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: anamo
rphic Hypocreales), are horizontally transmitted between colonies. Consiste
nt with theory of virulence evolution under this mode of pathogen transmiss
ion. Escovopsis is highly virulent and has the potential for rapid devastat
ion of ant gardens, leading to colony mortality. The specialized parasite E
scovopsis is more prevalent in gardens of the more derived ant lineages tha
n in gardens of the more "primitive" (basal) ant lineages. Because fungal c
ultivars of derived attine lineages are asexual clones of apparently ancien
t origin whereas cultivars of primitive ant lineages were domesticated rela
tively recently from free-living sexual stocks, the increased virulence of
pathogens associated with ancient asexual cultivars suggests an evolutionar
y cost to cultivar clonality, perhaps resulting from slower evolutionary ra
tes of cultivars in the coevolutionary race with their pathogens.