Defending against parasites: fungus-growing ants combine specialized behaviours and microbial symbionts to protect their fungus gardens

Abstract

Parasites influence host biology and population structure, and thus shape the evolution of their hosts. Parasites often accelerate the evolution of host defences, including direct defences such as evasion and sanitation and indirect defences such as the management of beneficial microbes that aid in the suppression or removal of pathogens. Fungus-growing ants are doubly burdened by parasites, needing to protect their crops as well as themselves from infection. We show that parasite removal from fungus gardens is more complex than previously realized. In response to infection of their fungal gardens by a specialized virulent parasite, ants gather and compress parasitic spores and hyphae in their infrabuccal pockets, then deposit the resulting pellet in piles near their gardens. We reveal that the ants' infrabuccal pocket functions as a specialized sterilization device, killing spores of the garden parasite Escovopsis. This is apparently achieved through a symbiotic association with actinomycetous bacteria in the infrabuccal pocket that produce antibiotics which inhibit Escovopsis. The use of the infrabuccal pocket as a receptacle to sequester Escovopsis, and as a location for antibiotic administration by the ants' bacterial mutualist, illustrates how the combination of behaviour and microbial symbionts can be a successful defence strategy for hosts.

Figure 1

Proportion of Trachymyrmex cf. zeteki colonies that built infrabuccal pellet piles after exposure to one of four infection treatments over a 48 h period.

Figure 2

Removal of the fungus garden parasite Escovopsis by Trachymyrmex cf. zeteki. Following infection, ants collect parasitic spores in their infrabuccal pocket via fungus grooming (a). In the pocket, Escovopsis spores are exposed to inhibitory antibiotics produced by actinomycetous bacteria (b). Once the pocket is full, the non-pathogenic contents are regurgitated in the form of pellets and stacked together in piles tended by the ants (c), leaving the fungus garden with tolerable levels of the parasite (d).