ALONE they鈥檙e nothing. Together, they鈥檙e the greatest double act in the
rainforest. The partnership between attine ants and the fungi that they grow in
their underground gardens is a huge success. Top billing goes to the
leafcutters, the most sophisticated of the Attini tribe. They remove more of the
vegetation in a tropical American rainforest than any other group of animals,
including mammals. Some experts estimate that leafcutters snip off as much as 20
per cent of the foliage a forest produces each year.
So what鈥檚 the secret of their success? Total commitment. The attine ants of
Central and South America and their fungal partners don鈥檛 just live together,
they have evolved together, each putting pressure on the other to change, to
improve the pair鈥檚 performance. Co-evolution has made ants and fungi
inseparable.
The first ant to take up fungus gardening probably accidentally discovered
that fungi growing on the bits of food it had stashed in its nest were more
nutritious than the food itself. It carried on bringing home rotting leaf
litter, not to eat but to feed the fungus, which it ate instead. Today there are
around 200 species of gardening ants. 鈥淢ost still take stuff from the forest
floor: dead flowers, bits of decaying leaf, caterpillar poop,鈥� says Ulrich
Mueller, an entomologist at the University of Maryland, College Park. The 20 or
so species of leafcutter have gone one stage further by harvesting fresh leaves,
stems and flowers.
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The attines and their fungi form a true symbiosis, with both partners
benefiting from the relationship. The ants exploit a type of food they can鈥檛
digest themselves. The fungi break down the indigestible cellulose of plants,
converting it into more edible proteins and sugars which their carers can
harvest. They also break down plant toxins designed to protect the plant against
insect attack. The ants, in turn, provide all the food the fungus needs,
avoiding plants that are bristling with antifungal chemicals. They chew leaves
to make them softer and more palatable, speed the fungus鈥檚 growth with manure,
provide shelter and weed out any rival fungi that sprout in the garden. Finally,
the ants disperse the fungi: when a new queen leaves the nest to start her own,
she takes a wad of fungus with her to create a new garden. 鈥淭he relationship
makes the fungi very successful,鈥� says Ted Schultz, an entomologist at the
National Museum of Natural History in Washington DC.
Ants first began to grow fungi around 50 million years ago, so both ant and
fungus have had a long time to work on the partnership. During co-evolution, the
partners drive natural selection, each putting some sort of pressure on the
other to change. 鈥淭hey are shaped by the relationship,鈥� says Schultz. The ants鈥�
food is predigested by the fungi, so they have lost some of their own key
digestive enzymes. They have gained glands to secrete chemicals that suppress
foreign fungi, and recent research suggests that their saliva contains
antibiotics to control harmful microbes. The fungus has also shaped the ants鈥�
behaviour, not just in developing their gardening skills but also in 鈥渢raining鈥�
them to select the best plant material.
Fast food
The fungi have changed too, with the ants driving natural selection every
time they choose a tuft of fungus to plant in the garden. 鈥淚f a new variant
arises鈥攁 mutation鈥攁nd if the ant finds it more attractive, it will
choose that,鈥� says Mueller. The fungi that live with leafcutters grow special
swollen, food-packed knobs called gonglydia on the ends of their filaments. 鈥淭he
ants pluck off groups of swellings to feed to their larvae or eat themselves,鈥�
says Mueller.
Four years ago, Mueller, Schultz and their colleague Stephen Rehner began to
trace the evolutionary history of the attine ants and their fungal partners by
examining their DNA. Because the fungus in each new nest is a clone of the one
in the parent nest鈥攃arried there by the new queen鈥攜ou might expect
all the species cultivated today to be descended from that first domesticated
fungus. According to this line of reasoning, as ants diversified into new
species, so should the fungi, and the family trees of ants and their fungi
should have an identical structure. 鈥淭he fungi would speciate as the ants
speciate,鈥� says Schultz. Until recently, however, no one could say whether this
really happened because the fungi hardly ever fruited, making them almost
impossible to identify.
Mueller and his colleagues genetically screened more than 500 fungi from
ants鈥� nests in Central America, and 300 wild fungi from the same region. They
found that leafcutters and their fungi do have very similar pedigrees. Once the
ants made the breakthrough to fresh foliage, about 23 million years ago, they
stuck with the fungi that could tackle such a difficult food. But there is not
such a neat relationship between the majority of older and more primitive
attines and their fungi.
The borrowers
Instead of a strict line of descent from one original fungus crop, the team
found that ants have domesticated fungi at least five times. Almost all the
cultivated fungi belong to a single family of tropical mushrooms, the
Lepiotaceae. But there is not a strict one-to-one relationship between an
ant and a particular fungus. Although a single ant colony grows only one species
of fungus, other colonies of the same ant species often grow something
different. One species of ant in particular grows eight different fungi.
Similarly, some genetically identical fungi turn up in the nests of different
species of ant, suggesting that one ant recently stole or borrowed the fungus
from the other.
The team also found two wild fungi that are genetically indistinguishable
from those grown by ants, indicating that these have only recently been
domesticated. One species of ant introduced to Florida earlier this century now
cultivates a local fungus. The newcomer probably arrived with its 鈥渙wn鈥� fungus
but this failed in its new environment. 鈥淪o it went to a native ant and got a
fungus that was adapted to local conditions,鈥� says Mueller.
The discovery that most attine ants don鈥檛 have an exclusive arrangement with
one particular fungus may be surprising, but it makes sense for both partners. A
strictly faithful relationship has brought huge rewards for leafcutters and
their fungi. But for a less advanced attine ant, with a small nest and tiny
garden, there鈥檚 a real risk that it will lose its fungus, perhaps through
disease. The ability to change partners means it needn鈥檛 starve to death. And if
it comes across a fungus that has been 鈥渋mproved鈥� by another species of ant, it
can take advantage of that. The fungi, for their part, have also kept their
options open, making themselves attractive not to a single ant but to a cluster
of species. So if one disappears, there鈥檚 always another to look after them.