High in the trees on the Fiji islands, ants in the species Philidris nagasau are doing something extraordinary. They've brought in seeds from several species of a large, lumpy fruit from a plant known as Squamellaria and carefully planted them in the nooks and crannies of the tree bark. Once the plant takes root in the tree and begins to grow, the ants climb inside its young stalks and fertilize it. But then the real action starts. As the fruit swells, the ants move inside, carving tunnels and rooms into the fleshy interior. When the colony expands, it may include dozens of these fruits, which look like strange tumors sprouting from tree branches.

Though researchers have known for a while that ant colonies can live inside fruits, a new study in Nature Plants reveals that this housing arrangement is far more complex and ancient than we knew. University of Munich biologists Guillaume Chomicki and Susanne S. Renner went to Fiji to observe the ants and found that they inhabited six different species of Squamellaria. Each of these species evolved to grow in tree bark using a specialized root system called a foot. When the plants are still young, the ants enter a small cavity in the stalk called a domatium to fertilize it. Though the researchers never directly observed how the ants did the fertilizing, they speculate that basically the ants are pooping in there.



As the plant matures, the domatium swells into an enormous, distended bulb shape. When it produces seeds, the ants plant them in other parts of the tree, guarding them as they grow. Given the choice between seeds from several Squamelleria species, the researchers observed that the ants would only plant seeds from their preferred species. One colony that the researchers observed was dispersed across 25 plants.

The ants continue to nourish the plants with fertilizer even after they are fully grown, and the plants provide them with sugary fruit as well as shelter. What's fascinating is that this is a true symbiosis between the two species. Chomicki and Renner could find no P. nagasau ants living outside the Squamelleria plants, nor could they find any of the ants' preferred species of Squamelleria spreading seeds without ant intervention. Genetic analysis allowed the researchers to reconstruct the evolutionary history of P. nagasau and their fruits of choice in Fiji. What they found was that the two species had probably been co-evolving for at least three million years.

P. nagasau's closest ant relatives build what are called carton nests, often molded out of wood fungus. Some carton nests hang from trees, and look very much like Squamelleria plants. But sometime around three million years ago, P. nagasau stopped building carton nests. At roughly the same time, Squamelleria evolved the "foot" root system that allowed the plants to grow on trees. The plants also developed the domatium structure where ants live. In related plants, both the roots and domatium would grow underground. It's very possible that many of the structural changes we see in Squamelleria came from careful ant cultivation, much the way humans changed the structure of beans and corn over thousands of years of farming.

P. nagasau aren't the only ants to become agriculturalists. Leaf cutter ants carefully grow fungus underground to feed their young, while Argentine ants shepherd vast farms of aphids in trees, milking them for a sugary substance called honeydew. What's different about P. nagasau is that its entire existence is dependent on the plant it farms. Squamelleria is in the same boat, depending on the ants to reproduce and flourish. Now we have greater insight into how that relationship developed. Millions of years before humans ever dreamt of farming, these insects had devoted their entire societies to growing cities made out of plants.

Nature Plants, 2016. DOI: 10.1038/nplants.2016.181

Listing image by Derrick J. Rowe