The Cuckoo Underworld

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Most birds make nests, and spend their time foraging to feed and care for their chicks. Cuckoos, on the other hand, don’t waste their time with any of that, they simply lay their eggs in another bird’s nest and let them do all the heavy lifting. This might sound like the easy option, but in fact cuckoos have made a whole lot more work for themselves trying to evade and deceive their neighbours. When cuckoos succeed in their trickery, their unsuspecting host suffers, producing fewer young that year and wasting time and energy. So, evolution has pitted host birds against cuckoos, with each side developing increasingly sophisticated techniques to try and get their own way. Host birds mob potential attackers, while cuckoos use mimicry to avoid detection, and threaten defectors with serious consequences.

Cuckoos are famous for taking advantage of their unsuspecting neighbours; laying eggs in their nest and leaving their unwitting host to raise the chicks. The world cuckold, used to refer to the husband of an adulterous wife, originates from the cuckoo bird. There are over 50 species of parasitic cuckoo in the family Cuculidae; some are generalists who will lay their eggs in any available nest, others specialise in one or a few ‘host’ species, but all are engaged in an evolutionary battle with the species they parasitise – an arms race, if you will. Species parasitised by cuckoos are at a disadvantage – in the best case they are merely wasting resources raising an unrelated chick, in the worst case the chick will hatch early and push out the other eggs in the nest, meaning that the unlucky bird in question loses an entire clutch. In each generation, therefore, natural selection will favour host birds that are able to avoid parasitism. The birds might evolve to be more discerning, for example, identifying the appearance of cuckoo eggs and removing them, or selecting nest sites that are more difficult for the cuckoos to access. Equally, in each generation the cuckoos that are most successful in deceiving and parasitising their neighbours will produce more offspring and their traits will be favoured by natural selection. Cuckoos might evolve eggs that more closely resemble those of their host, or very rapid egg incubation to ensure their chick hatches first. Ultimately, neither species wins, with evolution demanding increasingly sophisticated tactics for successful parasitism in cuckoos, and traits to thwart parasitism in the host species.

Another tactic to prevent parasitism is known as ‘mobbing’, in which neighbouring host birds such as the Reed Warbler gather together in large groups to attack approaching parasites. This tactic can be highly effective, but there are also risks involved. Joining the mob exposes an individual to predators and the consequences of failure. There is also the risk that the birds misidentify a predator as a parasite, and are instead eaten! In fact, scientists believe many cuckoo species have evolved to resemble predators such as sparrow hawks in order to make it more difficult for mobbing birds to be sure what they are getting themselves into. Some host species have therefore evolved to be more discerning about the targets of their attacks – in experimental trials, Reed Warblers refused to mob a parrot model but would aggressively attack a model cuckoo.

In Reed Warblers, there are individual differences in mobbing behaviour – some individuals are well up for a fight, others prefer more peaceful protests, simply removing cuckoo eggs when they find them. Recent research by Dr Davies and colleagues at the University of Cambridge has shown that this variation depends in part on how many cuckoos are around. In ‘high risk’ areas, where cuckoo parasites are common, Reed Warblers will mob an approaching cuckoo about half the time. And in these dangerous areas, this tactic works – cuckoos that join the mob are less likely to be subject to a cuckoo attack than their more peaceful neighbours. However, in areas where the risk of parasitism was low, mobbing was much rarer, and those individuals that did mob cuckoos were more likely to attract the attention of predators than scare away the cuckoo.

Social Learning


Mobbing behaviour is a strategy that has evolved in defence against brood parasites such as cuckoos, although its relative costs and benefits depend on the frequency of parasites in the area. Perhaps it is not surprising, therefore, that mobbing turns out to be a characteristic that is learned from other birds rather than preprogrammed – young birds only need learn mobbing behaviour if they find themselves in a high risk area. In 2014, Dr Davies and Dr Welbergen reported in the journal Science that young Reed Warblers (Acrocephalus scirpaceus) are afraid of cuckoos (presumably because of their resemblance to hawks), while older birds will noisily mob model cuckoos. Using a series of experiments with model cuckoos and parrots, Davies and Welbergen showed that warblers that had observed a simulated cuckoo attack on a neighbouring nest would be more likely to attack cuckoo models near their nest, and were more likely to join in simulated mobbings on neighbouring nests. It seems, therefore, that mobbing is a product of social learning – although the behaviour itself may be instinctive, its expression is shaped by the social environment.

One interesting finding in their research was that the warblers were highly selective about which birds to mob when their own nests were attacked – mobbing a model cuckoo but not the parrot – but did not show this level of selectivity when joining mobs defending other nests. When the researchers simulated mobbings on neighbouring nests with sounds and models, warblers were equally happy to join in to mob parrots and cuckoos! It is as though, when joining a mob that has already formed, the warblers simply assume that their neighbour has made a solid judgement.

Fear of the consequences


Egg mimicry is one obvious tactic that can make cuckoos better parasites. However, egg mimicry comes with a cost – it requires cuckoos to specialise on particular host species in order to mimic the appearance of their eggs. Although specialisation can be effective, it comes at the price of reliance on a particular host species, and therefore vulnerability to changing population dynamics of the host. If you specialise on parasitising a single species and that species goes extinct, you’re screwed. So, some species of cuckoo have opted to remain generalists, parasitising whichever bird species are locally abundant. But without the option of egg mimicry, cuckoos must find other ways to ensure their eggs aren’t rejected.

North American brown-headed cowbirds (Molothrus ater) have developed a clever tactic for ensuring their hosts comply. If the host bird rejects a cuckoo egg, they will retaliate by destroying their nest. This gives the host bird incentive to cooperate, and in areas where the cuckoos employ this tactic, host birds will play along and raise the cuckoo offspring alongside their own chicks. Far better to waste a bit of energy feeding one parasitic chick than lose your entire reproductive effort for the year! The Mafia Hypothesis was first proposed in 1979, and suggests that mafia-like tactics ensure cooperation, under the threat of punishment. Last year, researchers from the Max Planck Institute for Evolutionary Biology used mathematical models to test the hypothesis, and investigate the evolutionary dynamics of this unusual host-parasite behaviour. Because the strategy relies upon retaliation, learning is a crucial component – host birds must learn and understand the consequences of non-compliance. In their model, host and cuckoo behaviour was plastic, responding based on past interactions – the way in which behaviour and experience interact being determined through natural selection. The results showed that the frequency of mafia behaviour was cyclical, oscillating over time and never reaching an evolutionary equilibrium. In populations where the frequency of mafia behaviour in cuckoos was relatively low (and so the consequences rather unlikely), the best strategy is to be a little pragmatic, and only accept cuckoo eggs into your nest from cuckoos that have previously retaliated against you. Again, the social environment is key here, and cuckoos must learn which behaviour is best based upon past experience.

When host birds operate this conditional acceptance strategy (reject cuckoo eggs unless the cuckoo in question has previously shown mafia behaviour), evolution favours cuckoos that adopt the mafia behaviour. Because most birds will reject cuckoo eggs most of the time, the only way for cuckoos the ensure their parasitism is effective is to threaten consequences. Thus, the frequency of mafia behaviour increases in the population. However, when mafia behaviour is common in the population, the relative costs and benefits of different strategies change. For host birds, since almost all cuckoos are now part of the family, the best option is to just universally accept cuckoo eggs. Of course, when all host birds accept all cuckoo eggs, the mafia behaviour is rendered unnecessary and becomes rarer in the population. This is a classic example of how game theory (originally developed for economics) can be applied to evolutionary biology to help us understand how behaviour can evolve, change and cycle through time.

The cuckoos and their hosts are trapped in a never-ending cycle of mafia- and non-mafia-like behaviour in cuckoos and conditional and unconditional egg-acceptance in hosts. The authors suggest that, as a strategy to improve the success of parasitism, mafia behaviour may be better than egg mimicry because it avoids the need for specialisation and allows cuckoos to manipulate multiple hosts.

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