Rebellion! Enslaved ants fight back against their captors

Parasitism is the most common lifestyle on earth, be it plant, animal or fungi virtually all species are affected by it. There is something that I find deeply fascinating about parasites. It’s their adaptations that I find so interesting. Perhaps more so than any other type of organism, parasites have been fine tuned by evolution to fit their particular niches with exquisite precision. Some, such as mosquitos and ticks, may simply extract nutrients from their victims leaving them largely unharmed. Others, such as the ‘zombie ant’ fungus Ophiocordyceps unilateralis are much more sinister and can manipulate their host’s behaviour for their own selfish ends. Brood parasites are altogether different but no less interesting. Rather than using their hosts as a convenient food source these freeloaders exploit the parental care of others so that they don’t have to pay the costs of caring for themselves. Cuckoos, which lay their eggs in the nests of other birds, are probably the best known brood parasites but they are by no means the only species to have happened upon this particular lifestyle.

This image shows the slave-maker, P. americanus, on the left and the host species T. longispinosus on the right.
This image shows the slave-maker, P. americanus, on the left and the host species T. longispinosus on the right.

Slave-making ants are brood parasites which have evolved the ingenious trick of capturing and enslaving the workers of other ant species, putting them to work in their own nests raising their pupae. In many cases the slave-maker workers themselves have become completely unable to perform essential tasks on the colony such as foraging, nest maintainance and caring for their young. They have instead become specialised at searching for and attacking the nests of host colonies in slave raids during which all adult ants are killed or expelled. The slave-makers then rob the larvae of their host, taking it back to their own colony where they will develop into slave workers in the slave-maker nest.

Attacks by slave-maker ants are frequent and destructive and so impose a high cost on their hosts. This has led to the evolution of defence mechanisms in the host species which help it to resist enslavement, these include enemy recognition, fighting abilities and rapid escape from the besieged nest. All of these defences are useful before enslavement however, it has long been thought that defense behaviours that benefit the ants after enslavement could not evolve since enslaved workers cannot escape and, more importantly, cannot reproduce. Without a means of passing on their genes to a new generation it was thought that any new trait that arose in enslaved ants that helped them to fight back would die with those ants and be quickly lost.

This is the way that evolution normally works, new traits that are beneficial increase the reproductive success of the individuals possessing that trait and so, over time, it spreads through the population. Without reproduction a trait cannot usually spread. There is however another way. Animals can increase their own fitness by behaving in a way that increases the reproductive success of other animals with which they share a large proportion of the same genes. This is called inclusive fitness or kin selection and is in fact what worker ants do all the time. Worker ants are sterile but they can increase their own fitness by assisting the queen who carries a lot of the same genes that they do*.

So what does all this have to do with slave-maker ants? Well it seems that enslaved worker ants aren’t so helpless after all. Tobias Pamminger and his colleagues studied the relationship between the slave-maker ant, Protomognathus americanus, and its host, Temnothorax longispinosus. They collected colonies of both T. longispinosus and P. americanus ants from the wild and raised them in the lab. They then compared the brood rearing success of free-living T. longispinosus to their enslaved counterparts. Their results, which have just been published in the journal Evolutionary Ecology, show that enslaved worker ants actively fight back against their captors by killing or neglecting their pupae,  a trait termed slave rebellion. As the authors say in their paper…

Instead of raising the brood of their social parasite P. americanus to adulthood, enslaved Temnothorax were observed to kill a large proportion of the slave-maker pupae either by direct attack or by neglect

Enslaved ants attack pupae
Enslaved T. longispinosus attack the pupae of a slave-maker.

A startling difference was found in brood rearing success between the two groups. On average pupae in free-living T. longispinosus nests had a survival rate of 85% while for pupae in P. americanus nests, under the care of enslaved workers, this dropped sharply to only 45%.

Alternative explanations for this result were ruled out by the authors. One possibility was that conditions in the laboratory did not suit the slave-maker pupae resulting in high mortality. Another potential explanation is that the enslaved worker ants simply don’t provide the same level of care for the pupae of other species as they do for their own. Both of these explanations were rejected because the slave-maker larvae (the stage before pupae) developed normally with a high survival rate and were well cared for by the enslaved workers. In fact as the authors point out, larval stage ants require more care than pupae do and this was provided by the enslaved worker ants. It was only once the slave-maker larvae had reached the pupal stage that the slave rebellion trait was observed. In an earlier study the authors witnessed first hand healthy larvae being attacked and killed by enslaved workers. This is the smoking gun providing the final peice of evidence that the difference in pupal survival rates between the two species is not a result of the environment or general poor care but results from active attack behaviour by the enslaved worker ants.

A temnothorax sp. colony. Credit: Alex Wild.
A Temnothorax sp. colony. Credit: Alex Wild.

The results of this study clearly show that enslaved T. longispinosus workers attack and kill the pupae of the slave-makers, but how could a trait like this evolve when it is only used by sterile workers trapped in the nest of another species? Evidence suggests that kin selection is the answer. Genetic analyses revealed that in the wild, ants in nearby T. longispinosus colonies were closely genetically related to the ants enslaved in P. americanus nests. Tobias Pamminger and his colleagues suggest that by actively killing or neglecting slave-maker pupae the enslaved workers are able to reduce the size of nearby slave-maker colonies and so lower the risk of slave raids on colonies of their own species in the same area.

Here we have an example of kin selection in action. Although enslaved ants cannot reproduce and cannot directly benefit from killing the pupae of slave maker ants, they can benefit indirectly by reducing the impact of the slave-makers on nearby nests whose members carry the same genes that they do. This is they key point, natural selection acts on genes, not individuals. By behaving in a way they benefits copies of their genes in the bodies of free-living ants, enslaved ants were able to increase their own fitness and the slave rebellion trait was able to evolve.

*It’s actually a bit more complicated than this, ants have an unusual sex-determination system in which males carry only one copy of each chromosome while females carry two. This has all sorts of interesting implications which belong in a post of their own, see here if you’re interested.

                                                                                     

Pamminger T., Leingärtner A., Achenbach A., Kleeberg I., Pennings P.S. & Foitzik S. (2013). Geographic distribution of the anti-parasite trait “slave rebellion”, Evolutionary Ecology, 27 (1) 39-49. DOI:

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