Fungal Farming in Leafcutter Ants
In most cases, mechanism is an examination of the of the proximate physiological aspects of a behavior. However, the interaction of leafcutter ant colonies with fungal cultivars is an integrated network of different behaviors, not a single genetic pathway. This page looks at those elements of the colony that constitute and sustain the fungal gardens, focusing on divisions of labor within the colonies, reproduction, and multi-species symbiosis.
Mechanisms of Behavior
Leafcutter ant colonies are in general highly polymorphic, though there is significant variation between individual species. These descriptions are by no means exhaustive but are presented here to suggest the divisions of labor within the colony.
Figure 5. Various castes of the leaf-cutter species Atta cephalotes:(a) minim, (b) worker, (c) soldier,
Ants actively chew the leaves they harvest, deriving some nutritional benefit from the sap. They deposit the masticated leaves into special fungus chambers within their nests, providing a rich substrate. The fungus has difficulty penetrating the tough leaf cells walls, so this step is crucial in unlocking the nutrients within the leaves for fungi and ants alike. The fungus then secrete endo-protease enzymes which degrade pectin, facilitating the further decomposition of hemicellulose, cellulose, and starches to allow uptake for hyphal growth (12).
Mechanism of Fungal Farming
Across the spectrum of attine species, the transmission of the fungal symbiont between nests is vertical, clonal, uniparental, and only occasionally horizontal. Within the colony, propagation of the fungus occurs asexually, through the mycelial growth of a single-strain monoculture (1). It is believed that the symbiotic fungal species have been asexually propagated by leafcutting ants for millions of years (6). Ants, moreover, are very picky about the fungus they cultivate, and colonies are known to actively reject genetically different fungal clones in favor of their resident clone (1).
The queen is the only sexually reproductive female within the colony. Young queens leave the nest after mating with multiple males to begin new colonies of their own. Fungal reproduction is dependent on newly mature queens, who initiate new colonies by carrying fungal spores within their mouth, in a specialized space called the infrabuccal pocket, when they leave the colony to establish their own nest. In fact, this dependence is so entrenched that the Lepiotaceae fungi do not produce fruiting bodies to distribute spores and consequently do not engage in sexual reproduction (6). This phenomenon had long been held to be an incidence of sexual repression of the symbionts by their ant hosts, but research into long-distance horizonal transmission of symbionts has undermined notions of obligate clonality. While horizonal host switches are known to occur in congeneric taxa among primitive fungus farming ants, the so-called "lower attines", either directly between lineages or via free-living host species that act as bridges for transfer (10). Recent research has shown that the fungal cultivars of the upper attines, the leafcutter ants, also undergo horizontal transmission, suggesting that the co-evolution of ants and fungus is not reciprocally pairwise -- the fungus undergoes dispersal independent of their ant hosts, though the mechanisms are still unknown. Some scientists hypothesize that, in fact,, " a single widespread and sexual fungal symbiont species is engaged in multiple interactions with divergent ant lineages" (10).
More Complexity: Bacterial and Yeast Symbionts
Co-evolution does not occur only in mutualistic relationships but in antagonistic ones as well. Leafcutter ants, in creating a garden of Eden for their fungal cultivars, also play host to a parasitic microfungus of the genus Escovopsis, a virulent pathogen that dramatically reduces garden growth and colony growth in infected gardens (4). Specific species of ants are associated with specific cultivars, which are threatened by specific species of Escovopsis, a tripartate evolutionary congruence. In response to these pests, ants have evolved a mutualistic association with filamentous Pseudonocardia (family: bacteria that produce antibiotics effective against the Escovopsis pathogen.
In all attine species examined, modifications to the exoskeleton have evolved to house these beneficial bacteria. worker ants posess cuticular crypts in which to raise the Pseudonocardia, a modification absent in related but non-fungal-farming species of ant (4). The propleural plates of the attine ants contain crescent-shaped cavities, fovea, which house the antibiotic producing bacteria. Just below the fovea on the propleural plates, Currie et. al. discovered an exocrine gland composed of a gland cell and a duct cell. Additional bacteria-filled fovea cover much of the exoskeleton of the worker, including the head, thorax, abdomen, and legs, with the openings are covered by small microtrichia (hair-like cuticular projections). The position of the fovea on the cuticle depends on the species of ant and is believed to reveal broad trends in the evolution of ant-cultivar-bacteria mutualism (see Phylogeny).
Figure 7. Photograph depicting the bacteria flourishing on the propleural plates of Cyphomyrmex costatus (A). SEM images of the plates of Cyphomyrmex muelleri with (B) and without (C) bacteria (Fb) illustrate the position of the fovea and its hypothesized function as a specialized bacterial carrying compartment. [Image courtesy of Currie et. al. (2006)]
An additional component of the mutualism story is the presence of a black yeast (Ascomycota; Phialophora), which grows on the cuticle of the ant, localized to the propleural plates where the bacteria are cultured. Because the black yeast appears to constitute a derived monophyletic lineage that exists only in association with fungus-growing ants, it is hypothesized to be a fourth symbiont in the ant-fungus-Pseudonocardia mutualism, potentially with a role as saprophytes and oligotrophs, a function yeasts commonly fulfill in other ecological systems(9). Thus, the integrity of a leaf-cutter ant colony depends not only on the cultivation of fungi, but on a complex web of interrelationships between least four specie (five, counting the parasitic Escovopsis) out of which emerges the functioning whole.