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Antlion symbiosis story to make Darwin smile

by Rowan Hooper

Antlions, insects resembling feeble, intoxicated dragonflies, flutter briefly in summer, hardly eating, only copulating, reproducing then dying. But their life as larvae is all about food. Living for two to three years at the bottom of a funnel-shaped pit/trap in the ground, the antlion larva waits with open jaws for a smaller insect to fall in, whereupon it paralyzes its prey and sucks out its vital juices.

Now Kazuhiko Matsuda and colleagues at Kinki University in Nara have found that the larvae are in partnership with bacteria that live in the larva’s saliva and produce the paralyzing toxin, a protein of a class called chaperonins. The work, published today in Nature, provides an intimate example of symbiosis, where two organisms work in a mutually beneficial partnership, as well as of homology.

Homologues have long provided some of the most persuasive evidence for evolution from common descent. All te- trapods (amphibians, reptiles, birds and mammals) share a pentadactyl (five-digit) limb — a bat’s wing is structurally very similar to a whale’s flipper, a frog’s foreleg, a bird’s wing and a human’s hand. There is no reason why this should be, unless all these animals descended from a common ancestor.

The chaperonin that the partner bacteria makes for the antlion is also a homologue, as it originally had a completely different function. In all other organisms, the same protein helps protect other proteins from heat damage. In the antlion’s bacteria, chaperonin, slightly modified, has a different job: an insecticidal one.

The story is one Darwin would have liked, as antlions were one of the many animals that troubled him as a young man during his travels on the Beagle.

In Australia, Darwin observed (along with the extermination of the Aborigines) the antlion larva in its pit. The larva builds its pit by spiraling down into light soil, ejecting the debris with flicks of its head. It fastens itself into the soil at the bottom with forward-pointing spines, with only its jaws poking out. Prey, an ant or another small insect, wandering to the edge of the pit may slip and slide into the larva’s waiting jaws. If it somehow halts its slide halfway down the pit, the antlion larva fires sand at it, attempting to start the death slide again. Once sucked dry, the corpse is flicked out of the burrow. Antlions have no anal opening — they retain indigestible compounds in their bodies. At the end of the larval stage, some of the feces is used to spin silk for the animal’s cocoon.

Darwin had seen antlions doing the same thing in Europe. It was just this sort of observation that gave him sleepless nights.

“There can be no doubt,” he wrote in “The Voyage of the Beagle” upon leaving Australia and its antlions, “that this predaceous larva belongs to the same genus as the European kind, though to a different species. Now what would the skeptic say to this? Would any two workmen ever have hit upon so beautiful, so simple and yet so artificial a contrivance? It cannot be thought so: One Hand has surely worked throughout the universe.”

It would be many, agonizing years before Darwin accepted that it was no Hand, but natural selection that was at work.

And now, many years since then, the antlion is once again elegantly demonstrating Darwin’s ideas. Matsuda of the Pesticide Chemistry Laboratory at Kinki University and his graduate student Naofumi Yoshida, now also a researcher at the school, had the idea to isolate the bacteria in the saliva of the antlion Myrmeleon bore (Japanese name: Kurokosuba kagero). They cultured the bacteria, Enterobacter aerogens, and injected it into cockroaches. When the bacteria rapidly paralyzed them, the researchers knew it was something the bacteria was making, and not the antlion, that was the toxin.

They purified the protein from the bacteria and, by looking at its amino acid sequence (all proteins are made of amino acids), found that it was a homologue of chaperonin.

The homologue also paralyzed and killed cockroaches, whereas “normal” chaperonin from E. coli had no harmful effects. The researchers determined that the homologue differed from the E. coli chaperonin in a way that didn’t affect its protein-protection function.

In other words, a secondary function had evolved from the original function. Like the bat has a mammalian foreleg turned into a wing, the antlion’s bacteria has chaperonin turned into a toxin.