Saturday, 14 July 2012

Cuckoos – evolution of a parasitic arms race

There are over 100 species of cuckoo which show a wide range of breeding behaviours, but brood parasitism is extremely common, occurring in 59 species. This is where eggs are laid in another birds nest, so the cuckoo doesn’t have to build its own nest, incubate the eggs, or feed and protect the young until they fledge. The common cuckoo (a summer migrant in Europe and Asia which winters in Africa) is the most well know of these. How this mode of breeding first evolved, and how the cuckoo has adapted to maintain this parasitic strategy, are intriguing questions.

Evolving Brood Parasitism
There are many cases of peculiar reproductive cycles in the cuckoo family, which indicate possible routes for the evolution of cuckoo parasitism. In 2 New World species; the Smooth-Billed Ani and the Guira cuckoo, breeding occurs in groups using a single nest. They occasionally parasitize the nest of a neighbouring group. In the case of the Coucals, an Old World species, males are responsible for nest building and for incubating and feeding the young. The female has several clutches a year, often with various males. The females produce more clutches if there is a glut of food, and if she cannot find enough males with nests she lays in the nests of other birds. The owners of these nests may be fooled into incubating the eggs. These behaviours may be similar to those of parasitic cuckoos ancestors, and act as a precursor for a purely parasitic lifestyle.

Populations of birds parasitized by cuckoos have generally evolved to reject foreign eggs, but those not parasitized, such as birds in Iceland, do not show this behaviour. Therefore making the step from laying in nests of other members of their own species, to laying in nests of another species, may have been relatively easy. Maintaining this parasitism after the host species had evolved egg rejection behaviour must have been the real challenge. It has led to an ongoing evolutionary battle, which has lasted for around 10 million years and given rise to some fascinating adaptations. 

Egg Mimicry
A crucial adaptation has been egg mimicry, whereby cuckoos lay eggs of similar colour and patterning to the eggs of their host species. There is great variation in the level of this defence, for example the dunnock represents one extreme, lacking any egg rejection behaviour. As there is no evolutionary pressure in this case for egg mimicry, the cuckoo eggs laid in dunnock nests have a radically different appearance to those of the dunnock. Cuckoos tend to most highly parasitize those species which show a high level of acceptance of foreign eggs.

3 dunnock eggs, 1 cuckoo egg

The common cuckoo females fall into 15 groups or ‘morphs’ each of which mimics the eggs of a different bird species. Evolving multiple morphs is clearly advantageous. The number of nesting sites available to cuckoos is limited by the number of its host’s nests. Also if the cuckoos become too effective at parasitising their hosts, this will damage the host population size and further limit the future number of nest sites. By evolving a morph which mimics a previously unparasitised host species, the size of the cuckoo population can greatly increase. The first individuals of the new morph have little competition for nesting sites and are therefore very successful.

arrows showing cuckoo eggs

The egg shell is formed in the mothers oviduct and its pattern controlled by her genes. If she inherited the genes for shell colour and pattern from both parents, as in most bird species, then she could end up laying eggs which were a blend of different morphs. These would be rejected. An alternative would be for males to breed only with the corresponding morph of females, and this would cause the different morphs to gradually split into separate species (this does not seem to be the case). There is strong evidence that the different morphs are in fact sex linked traits; that is the genes specifying them are carried on the W chromosome (the sex determining chromosome in birds, passed from mother to daughter), so males can mate with any females without effecting the egg shell traits.

It is all very well to lay eggs that perfectly mimic an egg shell type, but how does a female know which species she mimics and therefore where to lay her eggs. For example does she lay a practice egg, and then go out on the hunt for similar looking eggs? One interesting study points at quite a different mechanism. Actually cuckoos quite often get it wrong, laying in the incorrect species’ nest. In these cases she is more likely to lay in a similar nest, than a nest containing similar eggs. It seems she is entirely unconscious of her cleverly disguised eggs, but is simply imprinting on the nest type she hatched in and choosing to lay there.

Lack of Chick Mimicry?
Whilst egg colour and pattern are closely mimicked, other aspects are not (at least in the common cuckoo). So for example the cuckoo eggs tend to be slightly larger and more rounded. It has been found that mimicking the egg size exactly doesn’t make the host more likely accept them. The larger egg size is an advantage to the cuckoo as it means a larger chick hatches, which can expel the other eggs from the nest. Another aspect that does not seem to be mimicked is chick appearance.

The type of mimicry adopted by the parasite is likely to depend upon the rejection mechanisms evolved by the host. So for example, in Australia, superb fairy-wrens have evolved to spot parasitic chicks. In response they desert their nest and start a new one elsewhere, a strategy used when the host is too small to remove the egg or chick. In this case the Horsfield's bronze-cuckoo chick is better than other brood parasites at fooling the superb fairy-wren. The scientists who have studied this example originally proposed it to be purely down to the ability of the cuckoo to mimic the call of the host brood. Recently they have found evidence that the Horsfield's bronze-cuckoo chicks also mimic their hosts visually.

In the case of Hume’s yellow-browed leaf warbler, it seems to have won its battle against cuckoo species (at least for now). As well as being highly aggressive towards adult cuckoos, it also expels their eggs, but is unusual in that it is not too bothered by what colour eggs it finds in its nest, but rather by the egg size. Its strategy is to reject any egg whose size differs from the others (Karen Marchetti has tried replacing all the eggs with larger mimics and in this case they are accepted). So why has the common cuckoo failed to mimic the egg size? Perhaps if a cuckoo matched its egg size to those of the warbler, the cuckoo chick would be too small to remove the hosts chicks, so reducing the benefit of the parasitism.

The means evolved by different host species to fight the cuckoos, and the means evolved by the cuckoo species to regain the upper hand, may depend on the specific costs that the defensive strategy has. If the host is too small to expel the cuckoo egg, but could take the strategy of moving nests and laying a fresh brood, this may pay off for some species but not for others. The presence of a cuckoo egg may not spell certain disaster as there is a chance it was laid too late and will hatch after the hosts chicks and fail to gain the upper hand. For host birds living in climates with a shorter breeding season, the cost of abandoning a nest may be high as they would be unlikely to raise the second brood. The strategy of abandoning a brood may also lead to the cost of the host bird mistakenly identifying their own chicks as cuckoos and deserting them. A further explanation of why hosts of the common cuckoo have not evolved chick rejection is explained by an idea called strategy blocking. That is that once one strategy has evolved (eg. egg rejection) then the cuckoo becomes a less effective parasite, and the benefit of adopting an additional strategy (eg. chick rejection) is greatly reduced.

Greedy Chicks
Features of the cuckoos which could have helped give rise to their parasitic lifestyle are the short incubation period of their eggs, and the short time it takes for the newly hatched chicks to become active. The cuckoo egg is retained for a longer period in the mother before laying, and it has recently been shown that this means the cuckoo embryo is at a later stage of development at the time of laying. Being larger and more developed than the host chicks allows the cuckoo chick to throw its nest-mates from the nest, to their death, and so most effectively parasitise the host parents. This aggressive behaviour may be a modification of normal chick behaviour, as chicks of many species with try to destroy their siblings is food is extremely short.

cuckoo chick expels a host egg

 Once a cuckoo chick has hatched, the host parents feed it at a similar rate as they would a whole brood of their own chicks. This is not due to the larger size of the cuckoo chick, as if a large blackbird chick is put in a small birds nest it is fed at the rate that a single host chick would be. The way it does this seems to be all in its call, the rate of which is at least as high as a whole reed warbler brood. This keeps its unfortunate host parents frantically feeding it. The reason that ordinary chicks haven’t developed this manipulative behaviour is probably a combination of the facts that they are genetically related to their parents, as opposed to the parasitic cuckoo, and also that if one chick called for food at a higher rate it would expend more energy, and increase the feeding of the whole brood, so gaining little advantage.

For the cuckoos and their hosts the evolutionary arms race rages on, in delicate balance. One or other may gain the upper hand, but their victories are never permanent.

Selected links:
Article by Ed Yong - Cuckoos mimic hawks to fool small birds
Pictures at BBC - How egg spotting birds catch out cuckoos
Video - The blind assassin

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