Bribing caterpillar sparks evolutionary arms race

The jungles of Borneo is where the Macaranga tree grows. These are thick, bushy shrubs with large tasty-looking leaves. But they defend these leaves from anything tempted to take a bite using an army of ants that they billet all over the tree in special hollow structures in their stems. They’ve also evolved sharp hairy projections, called trichomes, that are there to snag stealthy caterpillars that know how to befriend, bribe and slip past the ant army. But researchers in Cambridge have discovered that one particularly crafty caterpillar species, Arhopala amphimuta, has taken the arms race a step further and, as well as sidestepping the ants, also evolved a much thicker skin to brush past the otherwise lethal hairs. Ritabrata Chowdhury made the discovery while on fieldwork for his PhD. We got together at Queens’ College, where he began by telling me what these caterpillars look like…

Ritabrata - They would be very difficult to find because they hide on the underside of leaves and they're very nicely camouflaged and their patterns match the veins of the leaves to an extent and very simply they look like a flattened grape. That's what somebody told me when I showed them this.

Chris - Are they grape-sized? How big are they?

Ritabrata - They are actually grape-sized. They're almost like two to five millimetres, not too big, and the largest ones can go up to like a couple of centimetres.

Chris - They do sound like very hungry caterpillars then if they're that big. But where do they live?

Ritabrata - What sorts of leaves do they prey on? These are very hungry caterpillars and they are mostly found in Southeast Asia. The ones which I studied, I found on the island of Borneo and these ones specifically feed on macaranga trees. These macaranga trees are defended by ants. So these are very stinging ants. Every day when I used to work there, I would get stung by at least 100 to 200 ants. Not very nice for me, but I think I have now become a bit immune to it.

Chris - When you say the trees are protected and defended by the ants, so the ants will build a nest near the tree and they swarm all over the tree and if anything tries to eat the tree or you come along, you get attacked?

Ritabrata - The plants actually host the ants inside the hollow stem. So these are mutualists or they are symbiotic ants. The ants live inside the hollow bark, basically the hollow stem of the tree and the plant provides it with food. And in turn, the ants protect the plant from herbivores of all sorts. And if anything tries to come along, even if it's a monkey or something tries to climb on the plant, they will sting them.

Chris - Or you.

Ritabrata - Or me, of course. Of course me.

Chris - And these caterpillars, you're saying that they have got some way of surmounting this or getting past these ants?

Ritabrata - Absolutely. So what these caterpillars do is that they bribe the ants with sugar-like solutions which they make from special organs called myrmecophilous organs and this is a very strong characteristic of the group of these caterpillars or butterflies. These are lysinids or lysinidae and they have this ancestral tendency of coexisting with ants where the ants do not harm them and in some cases, the ants even protect these caterpillars because think about this, no predator can get to them. The ants will sting them away too. And in some cases, these special aropala caterpillars, to deal with the ants, they actually mimic, they have the same chemicals on their body so the ants actually think that they are part of their own. They think they're an ant.

Chris - So not only do the caterpillars feed the ants so they're making them happy because they're stupefying them with a big meal but they also smell like they do. Is that the tactic?

Ritabrata - Yes, that is the tactic. This is one of the processes that these special group of caterpillars utilise to deal with ants and live on trees which are covered with ants and feed on them. And now comes the very hungry part because the ants don't attack them they can just happily munch on as much as they want.

Chris - How have the trees responded? Because the trees have already invoked the ants to defend them this fends off most hungry caterpillars that haven't got this tactic. The tree must presumably be fighting back in some way. Is there any kind of evidence that the tree is defending itself in an additional way against these caterpillars?

Ritabrata - In most cases no but this is where my story comes in. It turns out one plant has now because their primary defence which is in the form of ants has been kind of counter adapted or been dealt with they have now come up with a new technique which is this one single tree from Borneo, the macaranga tree from Borneo, seems to have come up with sharp hooked hairs on its entire surface. And when caterpillars try to walk on these surfaces these are specifically for the caterpillars that can deal with the ants when they try to walk on them they get pierced and they die.

Chris - And that's just one species of tree or one tree specifically?

Ritabrata - There's one species of tree. So the Macaranga trees there are around 300 odd Macaranga trees all around the world and they range from almost from Southeast Asia to Africa and out of more than 300 species only one seems to have evolved this hook trichomes which possibly which we thought might be to deal with these caterpillars and that's exactly what we tested.

Chris - How do you know that it evolved to deal with those caterpillars or could it be that actually just it's a self-fulfilling prophecy it has that trait for some other reason and it's also helpful for stopping these caterpillars causing a problem?

Ritabrata - The evidence which goes in the favour is that it's just one single species which has this hook trichomes. If you would expect we call them trichomes or the hairs because you would expect this to be a strategy for like generalist herbivores a lot of them would have it. So this seems like a de novo evolution especially because the ants have already been dealt with in this case. So of course we can't prove this at the moment but this is the most concrete hypothesis that we have against it given that it's just a single individual species in Borneo that has been able to do this.

Chris - So you've got this really interesting evolutionary story here. The trees evolve, the caterpillars come along and surmount the ant defence. So the tree then evolves these spikes which will hit the caterpillar where it hurts, and then the caterpillars evolve ways to get round the spikes.

Ritabrata - Yes, that's exactly the story that we're looking at. There's just one single caterpillar species that sems to use these plants, and they can walk on them.