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Ants learned to farm 50 million years ago, way before humans did. Their crop of choice? Fungus. Meet the leaf-cutter ant. These ants carve out pieces of leaves and carry them back home (Figure 1). But the ants don’t eat the leaves themselves—they feed it to Lepiotaceae fungus they cultivate in their nests. The fungus breaks down plant polymers that the ant digestive enzymes can’t, making the plants nutritionally available to the ant hosts when the ants eat the farmed fungus (Figure 2). This ant-fungus symbiosis is thought to have originated in the Amazon basin, and since then has diversified into more than 250 species of ants that inhabit the Americas.

The fungus is the only food source for the leaf-cutter ant. If the fungus fails to thrive, the colony can bid farewell to life, and without their cultivators, the fungus also does not survive. In an , Ted Schultz, curator of ants at the Smithsonian National Museum of Natural History, says the fungus is “like a lot of our crops. We cultivate things that are so highly modified that they exist in forms no longer found in the wild.” Similarly, the leaf-cutter ant’s fungal crop is found only in association with the ants.

Maintaining the Crop

A fungal garden begins when a young queen starts a new colony. As she leaves the original nest, the ant takes part of the fungus with her, carrying it in her mouth until choosing the new colony location to lay her eggs. For the first month, the queen stays underground tending to the garden while she waits for her workers to mature. As with other social insects, the leaf-cutter ants divide the tasks needed to maintain the colony among them. When you look at worker ants from the same species, they often appear so different that they seem like they are two different species. Smaller workers care for the brood and farm the gardens while larger workers forage for leaves and maintain the nest. This polymorphism stems from both environmentally and .

Avoiding Contamination

The obligate co-dependence between the leaf-cutter ant and their fungal crop makes both species precariously susceptible to contamination events with other nearby microbes. How is this relationship maintained when decaying leaves make such a great feast for a multitude of microbes?

While fungi naturally produce antibiotics that can prevent the growth of some bacterial species, the ant’s behavior also explains the clean culture conditions. Ants are meticulous cleaners when it comes to caring for their crop. They remove debris and pest-infested areas in a process called weeding. Some ants even use separate areas within the nest as a waste dump to keep debris and contaminated portions of leaves or fungus away from their prized fungus gardens. Ants also “groom” their fungi, licking the fungus and selectively removing foreign fungal spores.

While leaf-cutter ants like to maintain a tidy abode, they also populate their fungal gardens with fecal droplets. This behavior is not out of carelessness, however; the droplets contain high levels of chitinases and lignocellulases likely that help promote plant degradation and the exclusion of fungal pests. Ants also secrete phenylacetic acid and short-chain fatty acids, both with antimicrobial properties. When the ants tend to their gardens, these secreted molecules are conveniently deposited to keep their crop pest free.

The Leaf-Cutter Ant Microbiome

While ants produce molecules to keep pests and invading microbes at bay, they also enlist several microbial partners to defend against pests. These bacterial mutualists have antifungal activities towards the garden’s most common fungal pests, but not towards the farmed fungus. The most well-studied example are the actinobacteria. Worker ants conveniently carry antibiotic-producing Actinobacteria species. Found on the underbellies of ants, the bacteria come in frequent contact with the fungus gardens. For some ants, the bacteria completely covers their bodies, giving them the appearance as if they were covered in powdered sugar (Figure 3). The association between Actinobacteria species and ants is likely due to from the soil.

While some ant colonies do succumb to fungal pests, many colonies thrive because invading fungi do not develop resistance to the antimicrobials produced by the bacterial mutualists. It is possible that because the leaf-cutter ants have many mutualists, it is difficult for pests to develop resistance to several antimicrobials at once. Though how the leaf-cutter ant mutualists maintain antibiotic efficacy is still a mystery, it is clear that the mutualism is here to stay.

Over time, fungus-farming ants lost the ability to make specific nutrients and . In some ways, the leaf-cutter ant’s fungus gardens act as an edible external digestive system. The mutualism between ant and fungus is continually evolving, and examples such as these demonstrate that ants have found ways to keep this mutualism alive for thousands of years.

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