Crafty cuckoos in coevolution arms race

All life evolves; in other words, changes in response to selective pressures from the environment. And some examples of evolution are extremely complex because they involve two organisms evolving in tandem: one is a parasite and the other is its host. So what are the rules of engagement in this arms race? Cambridge University’s Rebecca Kilner studies cuckoos; and working with colleagues in Australia, she’s found that what began as efforts just to imitate the host bird’s eggs has morphed - down under - into full blown imitation of appearances and sounds of the chicks instead…

Rebecca - Our research focuses on how evolution works. And the way that we do that is to look at pairs of species where one species is exploiting another. So we're trying to understand how one species adapts to exploit another species and how that second species adapts to avoid being exploited. And we're interested in understanding whether there are general rules in how evolution plays out in those circumstances.

Chris - And the obvious example must be the cuckoo because this is a bird that plants its egg in another bird's nest and gets the parent birds to then bring up an offspring chick, which is not their own.

Rebecca - That's right. And that's hugely costly for the parent that's looking after the cuckoo chick. They pay the price for doing that. They lose their own offspring. The cuckoo chick kills their own young soon after it hatches by balancing any unhatched eggs or newly hatched chicks in the small of its back and walking up the side of the nest and tipping them out. So the host bird loses its own offspring and then it pays again because it works really hard to look after an enormous cookie chick that it has no genetic stake in at the cost of being able to breed again in the future. What we are interested in finding out is how those arms races play out. Do they always go in the same direction across evolutionary time?

Chris - How can you tell that?

Rebecca - Perhaps I could provide some kind of previous context to this. So the study of cuckoos and their hosts has been going on for some time and was initiated in Cambridge by professor Nick Davies some time ago. And he focused his work on the common cuckoo, and its many hosts in the UK. And what he showed was that the arms race is very much focused on the egg stage. So cuckoos lay their eggs in the host nest like a reed warbler. The reed warbler carefully scrutinises its eggs, and if it sees an egg that looks a little bit different from its own egg, then it picks it up and throws it out. And in that way it can avoid being exploited by the cuckoo. And that defence has in turn selected for cuckoos that can better hide their eggs in the nest. And so they lay an egg that closely matches the host egg in appearance. Where our work comes in is on a completely different set of cuckoos, which live in Australia. They're called the bronze cuckoos. They're quite small compared to the European cuckoo that we are familiar with. And what we showed there was that there was no equivalent arms race happening at the egg stage. The cuckoo lays an egg that's approximately similar to the host's own egg, but if we were to put a model egg in the nest that looked very different then the host wouldn't throw it out. And it turned out that what had happened was that the whole thing had shifted onto the chick stage. Unlike the UK cuckoo, the Australian cuckoo had evolved a set of rejection rules that were focused at the chick stage and involved spotting the odd chick in the nest. And they're able to do that by listening to the calls made by the cookie chick and also by observing that it was a single chick by itself in the nest, which seldom happened when they were raising their own young. And so this combination of cues would lead the female to dismantle the nest while the chick was still alive and begging in the nest and to build a brand new one. And then the cuckoo chick would slowly starve to death over the next couple of days. And then immediately after it died, the meat ants would come in and dismember the corpse and carry it off to their nest and feed their young with the bits of the body. And meanwhile, the host has started a new nest and a new breeding attempt.

Chris - How do you know what the timeline is here? How do you know that it started with egg discrimination, 'your egg looks different to my normal eggs. I'm going to chuck it out' versus the, your chick looks different to my chicks in Australia. Was it that that was first and the eggs came second? Or do you think they all started with egg discrimination and the Australian version has moved on to chicks? How do you know that's the timeline?

Rebecca - We don't know for certain because we haven't lived for the millions of years over which this arms race has played out. But we can deduce it from a few clues. And the first is that the egg that's laid by the Australian cuckoo looks unlike the eggs laid by its close relatives and much more like the eggs laid by its host. So something has happened at that stage. It may have been that in the past the host rejected eggs just as we see happening in European cuckoos today. What happens now, we suspect, is that the egg contributes to the decision to abandon the chick. So we did all these egg experiments where we put an odd looking egg in the nest and observed no immediate reaction from the host. But once we'd discovered chick rejection, we went back to those experiments and we noticed that chick rejection was more likely if we had added an odd looking egg to the nest for one of our earlier experiments. So what we think is perhaps the hosts remember this weird egg and then they use it as part of their accumulated information about what's going on with their current breeding attempt when there's a chick in the nest. And that informs their decision to reject or to continue to feed the chick.