These workerless social parasites, sometimes called inquilines (from the Latin word for “tenants”), have a distinctive appearance that to human eyes easily sets them apart from their hosts. But their parasitic scheme succeeds because they have evolved ways to steal chemical odors from the host nest to camouflage themselves.

Genomic analyses have shown that ant inquiline species have independently evolved dozens of times, and nearly all of them parasitize a closely related species that looks and behaves as ants normally do. For evolutionary biologists, that posed a mystery: How could a new species of obligate social parasites evolve from its host species? If their ancestors had lived together in the same nest, they would have interbred too easily.

For many years, researchers hypothesized that the initial step had been reproductive isolation: that the early ancestors of the inquilines were normal ants that were reproductively isolated from their kin long enough to diverge genetically from them and become a new species. They could live on their own, but some of them eventually discovered the benefits of sneaking back into the nests of their ancestors for help. Their dependence on their hosts gradually increased, and they evolved from a state of optional or “facultative” parasitism to obligate parasitism.

The problem with that idea, Kronauer explained, is that nobody has ever observed in the wild what should be an essential, early step of the process: free-living, facultative social parasites living in isolation from their close relatives.

Trible and Kronauer’s new findings turn the previous assumptions on their head. Their alternative scenario focused on the pair of mismatched supergenes in the clonal raider ants. Sometime in history, one of those ants had experienced a mutation that replaced the supergene on one chromosome with a copy of the supergene from the other chromosome. The resulting mutant ant with two copies of the “parasitic” version of the supergene could have suddenly developed into a miniature queen that looked a lot like an inquiline.

The work showed that a single mutation in a supergene was sufficient to produce the full suite of changes observed in the obligate parasites, even before the ants were split by speciation.

“You can go from free-living to obligately parasitic in one step, and you don’t need to take a number of gradual steps involving a reproductively isolated facultative intermediate population,” said Trible, who is now at Harvard University. “What we can be sure of is that a free-living parent had a daughter who was immediately an obligate parasite.”

He continued: “That is the scenario that had never been entertained by any of the classical evolutionary theorists, because that’s the scenario that was thought to be too big of a jump for you to take.”

The fact that a single mutation can shift all of these traits in a single step “really changes the way we think about the evolution of these weird, workerless social parasites,” Kronauer said.

The Strength of Supergenes

Little is known about the evolutionary history of the supergene on chromosome 13 that confers the social parasite phenotype. However, it is unlikely to have evolved in a clonal species like the raider ants. “The clonal ants would have been the last place to look for supergenes,” said Michel Chapuisat, who studies ant supergenes at the University of Lausanne in Switzerland.

The reason is that all the ants in a clonal species are genetically identical: Random mutations aside, their genomes pass unchanged from parent to child. Something more complicated, however, happens in sexually reproductive species.

In the cells that produce eggs and sperm, the maternal and paternal copies of the chromosomes line up and swap corresponding segments of DNA. This process of “recombination” allows sets of inherited traits to be reshuffled randomly; without it, genes would be locked into the maternal or paternal lineages forever.

Because of recombination, genes for various parasitic behaviors could have been randomly brought together on chromosome 13. Natural selection would then have strongly favored the union of those alleles that worked well together. “If you have a parasite-determining gene, you can gradually put a bunch of other genes next to it that make [the ant] better and better at being a parasite,” Trible said.

Recombination might have eventually separated those genes again, but a fateful genetic accident intervened. Sometimes when chromosomes are being repaired after damage, a piece of DNA gets reinserted in an inverted orientation. Because inverted DNA can’t line up with its chromosomal counterpart, it can’t recombine, so any genes in the DNA are permanently locked together as a new heritable unit — a supergene.

That may be what happened on chromosome 13: An inversion in that 2.25-million-base-pair stretch of DNA could have locked together the traits for social parasitism as a supergene, which natural selection then maintained. Purcell noted that a lot of research surrounds other ways that a supergene like this one could have emerged, but “there’s such a strong benefit of having alleles that work well together, brought together into a region with low recombination,” she said.