Peaceful ant-plant partnerships lead to genomic arms races

Though these ants and their tree hosts have to work together to survive, their genomes still have to evolve quickly to keep the partnership solvent.

The Field Museum

Peaceful ant-plant partnerships lead to genomic arms races

It’s well known that humans—and our antibiotics—are in an evolutionary arms race with the bacteria that make us sick. As fast as we rev up a strong defense, they change to evade those defenses, upping the ante for either our bodies or our drugs. This arms race has been called the Red Queen hypothesis after the Alice in Wonderland character who told Alice that in looking-glass land, she would have to run as fast as she could just to stay in the same place.

But what about friendly alliances—such as those between us and the beneficial microbes that naturally inhabit our guts and other tissues and help us digest food and stave off other infections? Researchers have often assumed that once such a mutualistic partnership arose, both sides would be stable gene-wise—they would have no need to keep evolving to match each other. A decade ago, this idea was dubbed the Red King hypothesis. But a new study in ants finds that even partners known to be engaged in mutually beneficial associations have rapidly evolving genomes, apparently to keep those partnerships intact.

To find out how quickly friendly partners evolve, Corrie Moreau, an evolutionary biologist at the Field Museum of Natural History in Chicago, Illinois, and her graduate student Benjamin Rubin sequenced the genomes of seven ant species. Three survive by partnering with just one plant: the acacia tree, the Japanese knotweed, or a tropical tree called Tachigali. In the case of the acacia, Pseudomyrmex flavicornis defends the tree from elephants and other grazers in return for a special acacia-produced sugar and the hollow spines in which it nests. The duo also sequenced the genomes of three nonspecialist species—each closely related to one of the specialists—and one very distantly related ant species. All seven were in the Pseudomyrmex genus.

Rubin, now at Princeton University, compared the genome of each mutualistic ant with that of its partner and the distant relative, using the three sequences to calculate a rate of evolution based on the number of DNA differences between the distant relative and the other ants. “What we expected to see was a slowdown in the rate of evolution in the mutualist,” Moreau says.

But the opposite proved true. The genome of each mutualistic ant was evolving at a faster rate than that of the most closely related generalist, Rubin and Moreau report today in Nature Communications. Moreover, they discovered that changes were occurring in the same genes in all three mutualistic ant species compared with their nonmutualistic counterparts. Those genes included ones that shape behavior and affect the brain—logical, because partnerships depend on specific nesting, eating, and defensive behaviors, Moreau says. “The two partners must constantly dance together.” And because other pressures—such as disease or drought—could easily derail that dance, each partner must evolve quickly to make up for any missed steps. “I predict we will see it in lots of obligate systems,” Moreau says.

The work of Jacobus Boomsma, an evolutionary biologist at the University of Copenhagen, supports that prediction. Boomsma, who was not involved in the new study, looks at fungus-growing ants who have evolved interdependency with their crop. His team recently found that the genomes of such ants are changing the fastest of any genomes for which comparative data exist. “It’s encouraging to see this paper confirming high rates of evolutionary change with ants engaged in mutualisms,” he says. And François Lutzoni, an evolutionary biologist at Duke University in Durham, North Carolina, sees similar fast evolution in lichens, another intermit partnership.

The only DNA changes that Moreau and her team find hard to explain are those in genes tied to aggressiveness. The mutualist ants tend to be much more aggressive than the generalists—so much so that they will jump off a branch to attack her and her colleagues. But she and Rubin didn’t find evidence of sped-up evolution in genes tied to aggressiveness.

For Marc-André Selosse, a microbial ecologist at the National Museum of Natural History in Paris, it makes sense that the Red Queen hypothesis applies to mutualistic relationships as well as parasitic ones. “The emergence of cheaters can transform some mutualists into parasites at any time,” he points out. “So, Red Queen runs for everyone.”