First Known 'Social Chromosome' Found

To humans, all fire ants may look alike. But the tiny, red, stinging bugs known as Solenopsis invicta have two types of social organization, and these factions are as recognizable to the ants as rival football teams are to us. Researchers once thought that the groups' distinct physiological and behavioral profiles stemmed from a variant in a single gene. Now, a new study provides the first evidence that the gene in question is bound up in a bundle of some 600 other genes, versions of which are all inherited together. This "supergene" takes up a large chunk of what may be the first known social chromosome, analogous to the chromosomes that determine sex in humans.

The differences between the two types of fire ants start with the winged queens, according to evolutionary geneticist Laurent Keller of the University of Lausanne in Switzerland. A so-called monogyne queen is large, fat, and fertile. Once she's mated, she can fly long distances to start her colony, nourishing her eggs from her fat stores, and then wait until her larvae grow up into workers. A monogyne colony will accept only the original queen and kill any other that shows up; these ants are very aggressive in general. By contrast, a polygyne queen is smaller and needs mature workers to help set up a colony. Thus polygyne communities will accept multiple queens from nearby nests—unless, that is, one happens to be a monogyne, in which case, they kill her.

In 1998, working with entomologist and geneticist Kenneth Ross of the University of Georgia in Athens, Keller showed that the two groups of fire ants had distinct versions of a gene known as Gp-9. All of the monogynes had two copies of one form; among the polygynes, many had one normal and one mutated copy of the gene. At first glance, the finding made sense. The gene encodes an odor receptor that enables the insects to detect scents, so presumably the polygyne worker ants could smell a kindred queen. Ross and his colleagues cloned the gene in 2002.

But many researchers, including Keller and Ross, didn't think variations in a single gene could account for all the differences in size, fertility, odor, and aggression that separated the two ant groups. They wondered whether an inherited cluster of genes controlled these traits.

To look for such a cluster and find out how it might be passed down intact across generations, Keller and colleagues sifted through the DNA of some 500 offspring of monogyne and polygyne queens. (They had sequenced the fire ant's genome in previous research.) The investigators focused on the chromosome pair containing the Gp-9 gene. Their strategy, Keller explains, was to determine whether a group of genes in this area maintained its integrity by avoiding what's called recombination. In this process, the two copies of a gene (one from each parent) swap DNA sequences, ensuring that each offspring has a unique mix of genetic material. But if many genes are going to stick together through the generations, recombination can't occur.

Sure enough, in the fire ants, a group of about 600 genes surrounding Gp-9 showed a complete absence of recombination, the researchers report online today in Nature. The cluster takes up more than half of the chromosomes occupied by Gp-9; it includes most of the genes that account for differences between polygyne and monogyne groups. The team also discovered what might block recombination. The gene cluster contains an inversion, or a strand of DNA flipped end-to-end, making it impossible for recombined DNA segments to line up properly on the chromosomes and resulting in a hopeless genetic tangle.

Keller says this "social chromosome" arrangement mirrors that of sex chromosomes, which also don't recombine—ensuring that male animals, for example, will have the full set of male genitalia and none of the female structures. "It's not good to mix those up."

"This is a spectacular piece of work," says Ross, who was not involved in the study. "They've unlocked a whole new mechanism for how a supergene can determine something as complex as behavior."