Revolutionary ants kill the offspring of their oppressors

A study conducted by researchers at Johannes Gutenberg University Mainz (JGU) has revealed that enslaved worker ants improve the survival chances of their neighbouring relatives by killing the pupae of their oppressors.

The team examined populations of Temnothorax longispinosus worker ants in the United States that had been enslaved by the parasitic species Protomognathus americanus. Slave-maker ants such as P. americanus survive by forcing other species to care for their offspring. However, the researchers found that across three populations in the states of New York, West Virginia and Ohio, an average of only 45 per cent of the parasites’ pupae survived into adulthood. T. longispinosus ants were observed killing the offspring of their oppressors both via neglect and by actively tearing them apart. Whilst this behaviour does not directly benefit the saboteurs themselves, it does increase their neighbouring relatives’ chances of survival.

In 2009, JGU’s Prof Dr Susanne Foitzik became the first person to observe this rebellious behaviour within ant populations. She told ScienceOmega.com that the enslaved ants target their oppressors’ pupae because they are both easy to identify and unable to defend themselves.

"Adult slave makers are slightly larger than the slave workers," Professor Foitzik explained. "Attacking them, therefore, is not really an option because their captors are better fighters. Slaves do have the option of attacking their oppressors’ larvae but these larvae possess very few chemical markers. Ant communication is predominantly chemical and so it can be difficult for slave ants to recognise larvae not of their own species.

"Pupae pose the easiest targets for two main reasons. First of all, we detected the presence of certain chemicals on their surfaces. There weren’t many but they were consistently different from those of the host ants. We think that these chemicals can be used as cues to identify slave-making pupae. Secondly, pupae are quite soft and easy to rip apart. They are much easier to harm than the adult slave makers."

Although attacking their captors’ pupae does not benefit the host ants directly, it does increase their neighbouring relatives’ chances of survival. Does this behaviour, however, put the saboteurs in any danger? As Professor Foitzik explained, enslaved ants do modify their actions depending on whether or not one of their oppressors is present.

"We looked to see whether or not a slave maker’s presence in the nest made the enslaved ants less rebellious," she said. "Indeed, if you remove slave makers, you do find more killing than when they are present. However, we did not make any direct observations of slave makers noticing when their pupae were being attacked. This might be because pupae cannot call out for help. Moreover, the destruction of broods is quite a common occurrence within ant nests. Ants often produce more larvae than they can feed so at times when there is little food, they simply feed some and not others. For these reasons, slave-making ants are unlikely to notice rebellion taking place."

The findings of Professor Foitzik and her colleagues revealed that the survival rates of slave-making pupae differed significantly across the three populations that they examined. This result came as no surprise to the researchers, however, as it is in keeping with the geographic mosaic theory of co-evolution.

"Selection pressures vary between different locations," explained Professor Foitzik. "We conducted several experiments in which we exchanged parasite pupae between different ant populations and we discovered that parasite pupae are less likely to be killed by their local host than by a geographically-distinct population. Basically, this is because the parasite tries to mimic its local host. As I mentioned earlier, our chemical analyses revealed that the pupae don’t match their hosts perfectly. Even so, one would expect genetically-isolated populations to match one another to a lesser degree. The geographic mosaic theory of co-evolution states that selection pressures vary between different places. Also, in some populations, new mutations occur and help parasitic pupae to more effectively mimic the odour of their hosts. This results in fewer killings.

"Defensive capabilities also play a role here," Professor Foitzik continued. "For example, we found that West Virginian T. longispinosus ants were worse at defending themselves against the raids of slave makers than their New York counterparts. We genotyped colonies within the vicinity of the populations that we examined, and our results suggest that kill selection can explain the evolution of this behaviour. Essentially, if slave ants kill a parasite brood, the colony of their captors will grow at a slower rate and will conduct fewer and less destructive raids. Host nests in the vicinity benefit as a result. When we genotyped neighbouring populations in West Virginia, we found there to be many close relatives living within a close proximity to the host ants. Basically, rebellious behaviour is of greater benefit to neighbouring relatives in West Virginia than it is in New York. If you have fewer slave makers, you have fewer raids and your relatives in the next acorn are happier. There are numerous variations that exist between different ant populations, and these lead to slightly different trajectories in the co-evolutionary arms race."

Sabotage appears to be an effective strategy for increasing the overall chances of survival for certain ant species, but are these insects unique in terms of their rebellious tendencies? According to Professor Foitzik, such behaviours have been observed elsewhere in the animal kingdom.

"Similar behaviour has been observed amongst the hosts of certain cuckoos in Australia," she concluded. "Cuckoos lay their eggs in the nests of other species. Professor Nick Davies and his colleagues at the University of Cambridge have shown that many host species have developed egg recognition. They carefully check to see whether they have cuckoo eggs in their nests and if they do, they sometimes reject the nest and build a new one elsewhere. Surprisingly, the researchers rarely saw chick recognition. In most cases, if a host bird fails to notice the cuckoo egg, it raises the hatchling. This makes you wonder what the host bird is seeing because at many stages of development, cuckoos look significantly different to their hosts.

"However, there are certain birds in Australia that mimic the chicks of cuckoos. In these cases, host birds are able to recognise the parasite chicks and reject them during the latter stages. These cases are similar to our ant research. In my opinion, there are two stages of defence available to creatures that are exploited by parasites. The first is to try not to become enslaved. If ants are able to recognise a parasitic species, they can try to save their brood either by fleeing or defending against raids. However, if this doesn’t happen and the ants become enslaved, rebellious activity offers a second line of defence."