All queens, no workers: The evolution of socially parasitic ants
A small handful of ant species contain only queens and must sponge off other species to survive. New research on these social parasites offers insight into the ant caste system.
Life is unfair, especially if you’re an ant. In most ant species, females are divided into two castes: workers and queens. The queens are the only females who can reproduce, while a worker’s role is to collect food, defend the nest and care for the queens’ offspring. A worker typically dies after just a few months, whereas queens can survive for decades.
As harsh as the life of a worker is, it’s hard to imagine how they might escape their labours. Unless you want to starve to death, someone needs to put in the work.
But here’s the solution: it doesn’t have to be someone of your species.
When an ant invades a nest and uses its workers to help rear her own offspring, we call this social parasitism. Such behaviour can be observed in bumblebees, yellowjacket wasps, paper wasps and — of course — ants.
Invaders’ attitudes to their hosts can vary. The ant genus Polyergus, sometimes called “slave-raiding ants”, is particularly nasty. They’ve evolved to pick on the ant genus Formica. A Polyergus queen will invade a Formica nest, kill the Formica queen and have the Formica workers rear her brood.
Sometimes, the invading Polyergus queen will decide there aren’t enough workers in a nest. In a particularly cold-hearted move, the Polyergus queen will cohabit with the Formica queen for a while, then assassinate her housemate once she’s produced enough workers.
Other species are more subtle. Workerless social parasites have all the characteristics of queens—wings, big eyes, ovaries and an aversion to work. Just like Polyergus queens, they sneak into the nests of other ant species to find the workers they need to survive and reproduce. However, they prefer stealth over violence, and are happy to let the host queens live.
Take the shampoo ant, who disguises herself by catching ants from the colonies it wants to invade, licking them, then licking herself to gain their scent. She slips into the colony and produces offspring, who are raised by the host workers. Her offspring go on to either reproduce in the same host colony or find new nests to sneak into.
The evolution of layabouts
Evolutionary biologists have been speculating about the origins of socially parasitic ant species for well over a century. Even Charles Darwin contemplated the mystery.
For two groups to be considered separate species, they must be unable to reproduce with one another. Usually, that requires the species to be isolated as they evolve. If not separated, the two groups will interbreed and never diverge enough from one another to become incompatible.
Socially parasitic ants are closely related to their hosts, but it’s hard to understand how the groups branched off from one another when they live in such close quarters. Perhaps the mystery could be solved if only someone found an intermediate stage—ants that were only slightly socially parasitic .
At first glance, the clonal raider ant (Ooceraea biroi) seems like the opposite of a socially parasitic species. All clonal raider ants are workers, and they reproduce through parthogenesis—that’s Greek for “virgin birth”. The ants produce offspring who are nearly exact clones of themselves with no need for fertilisation.
While screening colonies of clonal raider ants in the lab, Waring Trible and colleagues discovered a series of rather odd-looking mutants. As pupae and immature adults, the ants possessed prominent, queen-like wings. They shed the wings upon maturity, but retained wing scars and the same body segmentation as queens. It was a ground-breaking discovery. No queens or winged ants had ever been observed among clonal raiders before.
The researchers conducted further experiments. Eggs from winged individuals were given to non-winged individuals to raise and vice versa. The offspring of winged individuals grew wings while the offspring of non-winged individuals did not. Excitingly, winged status seemed to be genetically determined.
Genetic analysis suggested that the queen-like mutation had recently evolved in the colony from which the researchers sourced the ants. No evidence was found of an intermediate stage. The queen-like ants seemed to have directly evolved from regular clonal raider ants. Since clonal ants reproduce asexually, interbreeding can’t prevent speciation.
The next obvious question was whether the mutant ants were queen-like in appearance only. Clonal ants are well-organised foragers. When a scout worker ant finds prey, it lays a pheromone trail back to the nest. Raiding ants then follow the trail to the prey. The researchers set up three types of colony: colonies consisting of only queen-like ants, colonies consisting of non-mutant ants and colonies that were an equal mix of both.
Although the colonies of queen-like ants conducted a similar number of raids to non-mutant colonies, the queen-like ants’ raiding parties were significantly smaller. In mixed groups, queen-like scouts initiated raids less often than non-mutant scouts, and queen-like raiders were less likely to participate in raids. Queen-like ants also produced more eggs than their nestmates.
The genetic factors that made the mutants look like queens also caused them to behave like queens. After so many years, Trible and colleagues had found the intermediate stage evolutionary biologists had been searching for.
There were downsides as well as benefits to being a queen-like ant. The mutants frequently died as they were emerging from the pupal case. Dead queen-like ants were often found with their pupal skin partially removed.
In colonies where queen-like mutants made up 10% or less of pupae, the mutant pupae survived 100% of the time. When queen-like mutants represented the majority of pupae, survival dropped to 50%. The researchers suggested that the mutants’ wings made moulting more difficult. They need workers to help them emerge from their pupal cases, and the workers can only help so many mutants at once.
It’s no mystery why workers always dramatically outnumber queens, why socially parasitic ants keep their numbers low in host colonies or why Polyergus queens time their assassinations so cunningly.
The queen gene
Remarkably, both queens and workers arise from the same set of genes. Every female embryo has the potential to become a member of either caste. The differences between queens and workers can be attributed to epigenetics—changes to the way the body reads genes rather than the genes themselves. Environmental signals like temperature, pheromones and larval nutrition put an embryo on track to develop as one caste or the other.
In an earlier study, Waring Trible and Daniel Kronauer discovered that caste was closely linked to size. On the whole, larger females possessed more queen-like traits. They proposed that caste is determined by body size, and factors that affect caste are simply factors that affect how large an ant grows. For example, increased nutrition results in a larger ant with a higher chance of developing into a queen, while starvation makes an ant more likely to become a worker.
But how do social parasites come into being? The speed with which queen-like mutants diverged from normal clonal raider ants suggests a simple genetic change.
Trible, Kronauer and colleagues sequenced the genomes of queen-like and non-mutant clonal raider ants. To link a trait to a specific mutation, biologists usually perform association studies —breeding individuals with and without the mutation to see whether they have the trait. But a classic association study isn’t possible in the asexually reproducing clonal raider ants. Instead, the researchers looked for differences between the two groups’ genetic sequences, operating on the logic that if queen-like traits are conferred by a certain genetic change, that change will be present in queen-like ants but no non-mutants.
As expected, there were only a few genetic differences between the two types of ant. 91% of those differences were located on chromosome 13, the second smallest in the ants' genomes. The researchers concluded that queen-like ants had evolved as the result of a single mutational shift on chromosome 13, which is suspected to contain a region known as a supergene.
Supergenes are clusters of neighbouring genes that are inherited together. They often contain several genes with similar functions that contribute to a shared characteristic — in this case, queen-like traits. Supergenes have been shown to affect ant sociality before. Last year, Eckart Stolle and colleagues showed that a mutation in a supergene region determined whether fire ant colonies had multiple queens.
It seems as though the difference between queens and workers lies in a single, tiny region of the ant genome.
This new study may have revealed the first step in the evolution of socially parasitic ant species. But it’s important to remember that not all socially parasitic ants will have evolved through the same means. These findings aren’t particularly relevant to nest usurpers like Polyergus.
Even if we only consider workerless social parasitism, this form of exploitation has independently evolved 40 times. We can’t assume the same mutations were responsible every time.