Ants: The First Farmers

We humans may pride ourselves on inventing agriculture, but we were not the first to do so. In one of the most extraordinary episodes of coevolution, one group of ants became mushroom farmers 50 million years ago. They remain hugely successful at agriculture today, and they have managed to avoid much of the grief we suffer with pests. We would do well to learn from them.

Fungus‑growing ants live in tropical forests around the world. In many species, a caste of large ants marches out from the nest each day in search of trees and bushes. They climb onto the plants and chew off pieces of leaves, which they bring home in a little green parade. The big ants pass the leaves to a smaller caste, which tear the leaves into smaller pieces. They pass them to an even smaller caste, which chew them into smaller pieces, and so on, until the leaves have been transformed into a paste. The ants then spread the leaf paste like a fertilizer on carpets of fungus in their nest. The fungus can break down the tough tissue of the leaves and grow, and the ants can then harvest special nutrient‑rich parts of the fungi. (Not all fungus‑growing ants fertilize their fungus with leaves many species search the forest floor for organic matter such as fallen flowers and seeds.)

The fungi that grow in the gardens of leaf‑cutter ants have become completely dependent on their farmers. Free‑living fungi propagate themselves by growing mushrooms filled with spores that are carried away by the wind. The garden fungi have lost the ability to sprout mushrooms. They are trapped in their ant nest, which they leave only when a young queen takes a bit of fungus in her mouth when she sets out to found a new colony.

The leaf‑cutter ants get a huge benefit from caring for their fungus. Ants can’t digest plant tissue, so most species cannot take advantage of the vast amounts of food that surround them. Leaf‑cutter ants can let their garden fungus do the hard work of breaking down leaves for them. And thanks to their partnership, the ants have become one of the most powerful players in tropical forests, eating a fifth of all the leaves grown each year in some tropical forests.

To understand how such a remarkable partnership evolved, scientists study the evolutionary relationships between the ants and the fungus. Since the 200 species of ants known to farm fungus are all close relatives (there are no nonfarmers in their ranks), biologists have long assumed that their saga must have begun with a single primordial lineage of ants inventing agriculture. They then passed the secret down to their descendants in every new queen’s mouth. As new species of ants emerged, their fungus would evolve into new species as well. If this was in fact the case, then the evolutionary tree of the fungus should perfectly mirror the evolutionary tree of the ants.

But the truth turned out otherwise. Since the early 1990s, Ulrich Mueller of the University of Texas and Ted Schultz from the Smithsonian Institution have been trekking through jungles around the world, gathering leaf‑cutting ants and their fungi. Back at their lab, they and their colleagues have sequenced the ant and fungus genes and used them to work out their evolutionary relationships. The ants did not domesticate a single original fungus. Mueller and Schultz have discovered that they have tamed fungi at least six different times. Once these six different lineages of fungi were domesticated, they branched into new species as their ant farmers have evolved into new species of their own. But on many occasions fungus species have been exchanged between ant colonies.

Mueller is now studying how these shifts take place. “One possible scenario,” he says, “is that pathogens wipe out entire gardens. Then the ants are forced to go to neighboring ants and steal a replacement, or temporarily join with them in one happy community. But occasionally we also see them invade a neighboring nest and wipe out the ants and take over their gardens.”

Thanks to Mueller’s work, ants now look more like human farmers than ever before. Our ancestors in China, Africa, Mexico, and the Middle East tamed a handful of plants and animals, a tiny fraction of the millions of wild species on Earth, just as ants domesticated a few of the hundreds of thousands of fungus species. As human cultures have made contact with one another, their crops have passed between them like fungal spores. The only major difference between us and the ants is that they stumbled across agriculture 50 million years before we did.

Leaf‑cutter ants have to struggle with pests just as human farmers do. In the case of the ants, several species of fungi live as parasites on their garden fungus. It’s possible for a spore of parasitic fungus to get into a garden and destroy it in a matter of days.

But Cameron Currie, who works with Mueller at the University of Texas, has discovered that ants use a fungicide to keep the parasitic fungus in check. The bodies of the ants are coated with a thin powdery layer of Streptomyces bacteria. The bacteria produce a compound that kills off the parasitic fungus while stimulating the growth of the garden fungus. Each of the 22 species of leaf‑cutting ants that Currie has studied carries its own strain of Streptomyces.

Judging from the fact that all fungus‑growing ant species that Currie has studied carry Streptomyces with them, it’s possible that the very first ones million years ago used them as well. And yet in all that time, the parasitic fungus has not evolved any significant resistance to the fungicide. How is this possible, when we humans have inadvertently bred resistant pests in only a few decades? Currie and his colleagues are only just beginning to tackle that question, but they have a working hypothesis: when we use a pesticide, we isolate a single molecule and apply it to an insect. But Streptomyces is an entire living organism that can evolve new forms of fungicides in response to any resistance that emerges in the parasitic fungus. In other words, ants are using the laws of coevolution to their advantage, while we end up turning them against us.

Evolution’s Widows

Coevolution can marry species together, but extinctions can turn them into widows. If a species goes extinct, its partners may have to struggle to survive on their own. Sometimes the struggle proves too much, and they ultimately become extinct themselves.

According to Daniel Janzen, a University of Pennsylvania ecologist who works in the forests of Costa Rica, a number of trees in the New World have been evolutionary widows since the end of the Ice Age. Many species of plants disperse their seeds by growing fruits. The fruits attract animals with their sweet flesh, and the seeds have evolved tough coats that let them survive the passage through the animals’ digestive tracts. The seeds can escape unharmed from the animals in their droppings, far away from the tree where they grew.

By getting away from their parent’s tree, seeds have a better chance of surviving. Seeds that simply fall to the ground are more likely to be eaten by the beetles that linger under trees; even if the fallen should manage to sprout, they have to struggle under their parent’s shade. And dispersing seeds is also good insurance against extinctions: if a hurricane should wipe out one stand of trees, their offspring a few miles away may be spared.

Just as orchids adapt themselves to particular kinds of pollinators, many plants adapt their fruits to attract certain kinds of animals. Some fruits with brightly colored skins catch the eyes of birds; the fruits that depend on bats and other nocturnal animals with poor color vision instead have rich aromas. But as Janzen has pointed out, some fruits make it difficult for any living animal to disperse their seeds. In Costa Rica, where Janzen works, the seed‑dispersing animals include bats, squirrels, birds, and tapirs. None of them can eat the fruit of the tree Cassia grandis. Cassia produces fruit a foot and a half long, with seeds as big as cherries embedded in a fibrous pulp, encased by a woody hull. Because no living Costa Rican animal eats the Cassia fruit, it simply hangs on the tree until beetles drill their way into it and destroy most of the seeds.

The fruits that grow on Cassia and many other New World plants may be too big, hard, or fibrous for living animals to eat, but they would have been a perfect meal for giant ground sloths, camels, horses, and many other large mammals that went extinct 12,000 years ago. These animals had mouths big enough to take in the fruits, and teeth powerful enough to open them. For millions of years, Janzen argues, the giant fruits had coevolved with giant mammals. While other plants adapted their fruits for birds or bats, these plants depended on the megafauna.

Big mammals in the Old World still have this relationship with some plants–Sumatran rhinos, for example, feast on mangoes and pass their giant seeds in their dung. The hard shells and fibrous pulp of the Costa Rican fruits are a major obstacle to a small animal like a bird, but for a ground sloth it would be easy eating. A sloth would graze under the trees, sniffing for ripe fruits that had fallen to the ground. When it came across one, it would pop the entire fruit into its enormous mouth and crush the shell with its massive molars. While it chewed lazily on the pulp, the big seeds–which are usually coated in oil–would slip down into its giant gut. Later, after the sloth had shambled a few miles away, it would release the seeds in a giant plop of dung, where they would sprout into saplings.

The forests of Costa Rica were not unique during the Pleistocene: fruits were probably coevolving with giant mammals throughout the New World. Janzen has proposed that many other plants, such as avocados and papaya, are likewise widowed. When the giant mammals disappeared, these plants suffered a devastating loss. In some cases, their seeds could still be spread by smaller surviving animals, such as tapirs or seed‑hoarding rodents, but their dispersal became far less reliable as more of their seeds were devoured by mice and insects. Many species became rare, as individual trees died out without being replaced.

The arrival of the Spaniards, bringing with them horses and cattle, went a small way toward restoring the Pleistocene ecology of the New World. These big mammals love to eat the widowed fruits. One Costa Rican fruit called the jicaro has a shell so hard that people use it for making ladles; Janzen has found that horses are the only animals living today in Costa Rica with a bite strong enough to crack it. They will do so happily, and after they’ve eaten the fruit inside, jicaro seeds survive the passage through their gut and sprout from their dung. Before the Spanish brought horses to Costa Rica, the jicaro was trapped in its own hard‑shelled prison. While horses and cattle may ravage the New World wilderness in other ways–by trampling fragile soils and overgrazing grasslands–they can nudge plants like the jicaro a small way back to their Ice Age glory.

The extinction of the great mammals of the New World left behind trees that had long depended on them to spread their seeds. Except for what little help they’ve gotten from introduced livestock, Janzen argues, these widowed plants have been ebbing away over the past 12,000 years as their ranges shrank. Now, as the extinction rates accelerate, we may be creating a new generation of evolutionary widows.

These widows may come to include some of our own crops. Agriculture relies on pollinating insects for its existence, but humans have besieged pollinators over the past few centuries. Before Europeans arrived in North America, there were tens of thousands of pollinator species, including bees, wasps, and flies. The colonists brought with them honeybees from Europe, which they kept in managed hives. The honeybees competed with native bees for a limited supply of nectar, and their managed hives–with their reliable supply of honey–gave them a competitive edge. Bernd Heinrich of the University of Vermont has calculated that a single honeybee colony can wipe out 100 colonies of native bumblebees. An untold number of native pollinators have gone extinct, and many of the survivors are endangered.

Honeybees are now in decline as well. Pesticides have been ravaging their numbers, and parasitic mites recently introduced into the United States are killing off entire colonies. In 1947 there were 5.9 million honeybees in managed colonies, but by 1995 they had fallen to less than half that number, at 2.6 million. Feral honeybees have almost completely disappeared. If honeybees vanish, farmers will have to rely on the native species to pollinate their crops, but the natives may no longer be around.

It’s easy to pretend that humans are the champions of the evolutionary race, that through some kind of superiority we have won Earth for ourselves. But in fact whatever success we enjoy depends on the balance between ourselves and the plants, animals, fungi, protozoa, and bacteria with which we have been coevolving. If anything, we are the most coevolved species that has ever existed, and depend more than any other species on the web of life.

Nine

Doctor Darwin