Pest control for ants
(Top) A small leafcutter worker atop a leaf guards her sister against attacks by parasitic flies. Ants carrying leaves cannot use their mandibles for defense, so they carry hitchhikers to ward off the parasites. (Bottom) The fungus garden in a nest of Atta leaf-cutter ants. Notice the diversity of ant sizes within a colony, from the large red soldier ants to the minute orange ants tending to the garden. Atta ants have some of the most sophisticated caste systems among the social insects. -- photos and captions from Alex Wild (mymercos.net)
This week’s paper, “Black yeast symbionts compromise the efficiency of antibiotic defenses in fungus-growing ants" by Ainslie Little and Cameron Currie, was just published in Ecology. Elsa Youngsteadt interviewed me, among others, for a story in Science about this research.
I’ve never done research on the fungal “farms" of ants and termites, but I’ve been interested in them every since a camera company bought a close-up photo (not Photoshopped like this one) of an ant carrying a leaf along a barbed wire “bridge" on its way back to its nest, from my mycologist father, William Denison. Dad was best known for pioneering research in the tops of tall trees, but never had to fight a shaman, as far as I know.
The ants feed harvested leaves to fungi, then eat the fungi, so a feedlot might be a better human analogy than a farm. (Fungi are more closely related to animals than to plants.) The fungal “crop" (or “herd") can be attacked and destroyed by a second fungus, Escovopsis. (Wolves?) But Escovopsis is controlled by antibiotics produced by bacteria that live on the bodies of the ants.
Ever since I first heard about this, I’ve wondered, “what benefit do individual bacteria get from making the antibiotics?" Sure, collectively the bacteria and the ants are interdependent. But mutant bacteria that don’t make antibiotics (thereby saving some energy) must arise all the time. If the benefits of a healthy ant colony are just as available to these mutants as they are to antibiotic-producers on the same ants, then we would expect “cheating" mutants to take over the surface of each ant, whatever the long-term consequences. Bacteria don't plan ahead.
This week's paper introduces a new player that may hold the key to this question: a yeast (single-cell fungus) that lives on the ants, along with the bacteria. In culture dishes, the yeast grew more when bacteria were present, and the bacteria survived less when the yeast was present. So it appears that the yeast is, in some sense, “eating" the bacteria.
In the short term, therefore, the yeasts may be harmful to the ants. Escovopsis caused more damage to the ants’ fungal gardens when the yeast was present.
But is it possible that yeasts have an evolutionary effect that benefits the ants? If antibiotics that kill Escovopsis also have some protective effect against yeast, then there would be an individual benefit to antibiotic production that would select against “cheating" mutant bacteria that don’t produce antibiotic. The fact that antibiotic-producing bacteria still have a net positive effect on the yeast doesn’t undermine this hypothesis; the question is whether mutant bacteria that don’t produce the (Escovopsis-killing) antibiotics are hurt more by the yeast than antibiotic-producers are.
There is a good precedent for this hypothesis. Some bacteria that live on plant roots make antibiotics that protect the plant from fungal attack. In 2003, some colleagues and I pointed out (also in Ecology) that this raises the same question as the antibiotic-producing bacteria on ants: “is there some individual benefit that selects against nonproducing mutants?" It turns out that the antibiotics protect individual bacterial cells from being eaten by protozoa, in addition to helping them compete against other bacteria. I suggest that black yeasts on ants might play an analogous role to the protozoa near plant roots: imposing individual selection for antibiotic production that also happens to provide a collective benefit.
The authors of this week’s paper don’t mention this hypothesis and there are may be other explanations. Ulrich Mueller, another expert on ant agriculture, suggested in the Science story that by transplanting only (the most productive?) part of a fungal garden, ants are “selecting on an entire community that has desirable characteristics." If so, this could be a genuine example of “group selection" in nature.
But the antibiotic-producing bacteria live on the surface of the ants; they aren’t part of the garden. Therefore, for group selection to counteract loss of antibiotic production, the unit of selection would have to be the ant. Do ants whose bacterial populations stop producing antibiotics remove themselves from the colony, for the benefit of their mother and sisters? Do their sisters kick them out? I expect we will have answers to these questions some day.
Watch for a chapter on ant agriculture in my book, Darwinian Agriculture, which should be published in 2009.