The rebellion of the ant slaves

Blogging on Peer-Reviewed ResearchHumans aren't the only species that have had to deal with the issue of slavery. Some species of ants also abduct the young of others, forcing them into labouring for their new masters. These slave-making ants, like Protomagnathus americanus conduct violent raids on the nests of other species, killing all the adults and larva-napping the brood.

i-419dff83ab4f2419c0b5d46c21c3a326-Ant.jpgWhen these youngsters mature, they take on the odour of their abductors and become the servants of the enslaving queen. They take over the jobs of maintaining the colony and caring for its larvae even though they are from another species; they even take part in raids themselves. But like all slave-traders, P.americanus faces rebellions.

Some of its victims (ants from the genus Temnothorax) strike back with murderous larvae. Alexandra Achenbach and Susanne Foitzik from Ludwig Maximillians Universty in Munich found that some of the kidnapped workers don't bow to the whims of their new queen. Once they have matured, they start killing the pupae of their captors, destroying as many as two-thirds of the colony's brood.

Ants that are targeted by slave-makers take massive hits to their colonies and they are under intense pressure to resist these marauders. But all the defences discovered so far happen before the raids have been successfully completed. They involve better fighting skills, quicker reaction times when enemies are spotted, hastier escapes and so on.

Some scientists have suggested that strategies like this would be impossible to develop because the enslaved workers are caught in an evolutionary trap. Far away from their own colony, and sterile themselves, there is no way for them to increase their reproductive success. But Achenbach and Foitzik have rejected this idea - their conclusion is that by conducting assassinations within their new home, they severely reduce the slave-makers' numbers and their ability to conduct raids. That safeguards the future of their relatives.

Achenbach and Foitzik collected 88 colonies of the slave-making P.americanus ant that had abducted workers from three species of Temnothorax. They found that the workers clearly care for the larvae, and nearly all of them were raised until their pupated. But at that point, the slaves' behaviour changed dramatically, taking on a more homicidal bent.

Two-thirds of pupae died before they hatched. The mortality rate was even higher (83%) for pupae containing queens, but very low (3%) for those containing males. The duo saw that the captives were deliberately killing the healthy pupae. In about 30% of cases, as in the photo, the workers would gang up to literally pull the developing ants apart. Another 53% of the pupae were killed by neglect, by workers who moved them out of the nest chamber.

These murders were solely the acts of the slaves. No P.americanus worker ever lifted a mandible against its own pupae. Nor are the deaths a reflection of a generally poor standard of care on the part of Temnothorax. In their own colonies, the majority of pupae hatched, with just 3-10% dying before that happened.

This rebellion takes its toll on the slave-makers and may explain why the nests of P.americanus tend to be very small. The captives may never reproduce themselves, but they do their part for their relatives back home by crippling the workforce of the slave-makers. These indirect benefits are particularly pertinent to Temnothorax ants because a single colony can occupy many different nests - a family of sisters spread out over a large area. If one nest is raided, it pays to ensure that none of the related nests are targeted later.

Other species use similar strategies to reject attempts by parasites to usurp their parental efforts. For example, cuckoos all over the world lay eggs with varyingly strong resemblances to the eggs of other birds, in an attempt to turn them into unwitting foster parents. Hosts develop sharper recognitions skills and cuckoos develop more strikingly matched eggs. In Australia, this arms race has escalated to the point where the superb fairy wren has adopted a different strategy - it ignores the egg and recognises the young bird, killing it if it turns out to be a bronze cuckoo.

At the moment, P.americanus is on the losing end of a similar evolutionary arms race with its hosts. But it's an old parasite with a long history with Temnothorax. Achenbach and Foitzik believe that the rebellious slaves are a recent countermeasure against the problem of slavery and the impetus to evolve resistance is now on the slavers. They need to develop counter-adaptations to prevent most of their brood from dying at the jaws of their captives. The war is not yet over.

Reference: Achenbach, A., & Foitzik, S. (2009). FIRST EVIDENCE FOR SLAVE REBELLION: ENSLAVED ANT WORKERS SYSTEMATICALLY KILL THE BROOD OF THEIR SOCIAL PARASITE

Evolution, 63 (4), 1068-1075 DOI: 10.1111/j.1558-5646.2009.00591.x

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Wow--fascinating. And it's so interesting that animal behaviour that is advantageous for other members of the species, though not for the individual, persists.

I thought this may have been an April Fool's until I saw the reference checked out. Amazing things these ants are capable of!

Some scientists have suggested that strategies like this would be impossible to develop because the enslaved workers are caught in an evolutionary trap. Far away from their own colony, and sterile themselves, there is no way for them to increase their reproductive success.

But you make that objection to many altrustic acts. I thought the selfish gene paradigm would have ended that type opf thinking.

By Marc Abian (not verified) on 01 Apr 2009 #permalink

That should be "you CAN make that objection", as in anyone can. I wasn't accusing Ed of making any such objections.

By Marc Abian (not verified) on 01 Apr 2009 #permalink

This is very interesting.

Normally evolution is thought of as being competition among individuals.

The fact that we are altruistic requires us to expand the idea of evolution to groups.

Here we actually have evolution at the level of competition between species. That is, individuals are acting in a fashion to benefit their specie, rather than just themselves or their colonies (assuming that their destruction of the Protomognathus americanus benefits their entire species rather than just their own colonies).

How does this evolution that benefits the entire species work? This is not simple. If an individual (colony) develops a trait that is detrimental to Protomognathus americanus, how does that trait grow within the specie? It is after all not obvious that this trait should survive competition within the specie. A colony that has this trait, does not have an advantage against other colonies of the same species which are competitors for resources.

A specie that has this resistance trait will be successful, but explaining how the trait grew within the specie is not simple.

The long term equilibrium cannot be where Protomognathus americanus are excessive, as they depend on other ant species for survival. Their fraction of the total ant population (of all species) cannot increase beyond a point. This co-existence probably provided enough time for other species to develop the resistance.

I, too, thought it was an April Fool's joke when I saw the title. "Rebellion of the ant slaves"? Sounds almost as implausible as the comic strip I saw some time ago that showed "enlightened ants" who refused to enslave other ants. And yet, it's true! Astonishing!

It does, indeed, make evolutionary sense, kin-selection and all, yet, it's still a rather impressively complex behavior to be developed in such a way.

@Jayanta:

The direct benefits are not at the level of the species*. The ants' home colonies are still around, and benefit from their enslaved members' actions. The slaves are benefiting their sisters back home. Ant colonies are large families, all with the same parents, generally sharing ¾ of their genes. Thus, the genes that result in this rebellion are likely to be shared by others in their home colony. The survivors in the home colony thereby benefit, and spread out.

*There is likely to be some benefit to unrelated colonies. However, this is an evolutionarily neutral situation, as the benefit to unrelated colonies is not actually depriving their home colony of benefits, particularly as the closest nests to the P. americanus colony are likely to be the slaves' home colony, and thus, they are the ones who receive the greatest benefit

"Some scientists have suggested that strategies like this would be impossible to develop because the enslaved workers are caught in an evolutionary trap. Far away from their own colony, and sterile themselves, there is no way for them to increase their reproductive success."

This makes more sense if you do not consider the worker ants as individual organisms. They are, after all, created by their queen to serve her purposes, and, being sterile, have no evolutionary interests of their own to look after. Saying that they are "in an evolutionary trap" and therefore have no reason to act against their captors is similar saying that the toxins of a poisonous beetle which has been ingested by a predator are "in an evolutionary trap" and have no reason to poison their captor.

By Ben Morris (not verified) on 02 Apr 2009 #permalink

Paper Hand wrote "The direct benefits are not at the level of the species*. The ants' home colonies are still around, and benefit from their enslaved members' actions."

Thanks, there has to be something like this going on for this evolution to succeed. Maybe groups like this which had this, went on to expand till they became the entire specie.

Ben Morris wrote "This makes more sense if you do not consider the worker ants as individual organisms. They are, after all, created by their queen to serve her purposes, and, being sterile, have no evolutionary interests of their own to look after."

I agree. As I wrote in this post a couple of days back: A better comparison would be comparing (worker and other non-reproducing) ants to the white blood cells in your veins, which will attack bacteria without hesitation, though it may lead to their own destruction.

Alex wrote: For those with access to the Chronicle of Higher Education, myrmecologist Joan Herbers provides a worthy criticism of the terminology of ant slavery:

I remember when this article came out, and there's a nice response by James Trager available on line as well:

http://www.notesfromunderground.org/archive/april%202007/opinion/trager…

I learned the coinage "dulosis" early in my entomological education, and (unlike Herbers) I prefer that term, but I think Trager also makes a good case for "cleptergy", which means "theft of work."

By Julie Stahlhut (not verified) on 02 Apr 2009 #permalink

"Normally evolution is thought of as being competition among individuals."

I remember on the first day of Genetics my professor really, really drove home that evolution is about populations and not individuals. The individuals may be the source of the mutation, but populations evolve as that spreads.