Driving parents cuckoo

Do nestling birds signal their food needs honestly to their parents? A study of begging reed warblers shows that they do, but that parental sensitivites to vocal and visual cues can be exploited by an invading cuckoo chick.

The distinction between wants and needs lies at the heart of thinking on how dependent offspring communicate with their parents. Does a newborn send accurate and truthful information about its nutritional requirements, thereby helping its parents to allocate limited resources for the good of the whole brood? Or does it (unwittingly) practise deception, using ‘psychological weaponry’1 as a foil against its parents' physical superiority, and manipulating them into skewing investment towards itself at the expense of its nest-mates?

A quarter of a century ago, R. L. Trivers' influential theory of parent-offspring conflict1 challenged biologists to stop thinking of offspring merely as ‘passive vessels’. Several theoretical approaches have since been used to model this parent-offspring conflict2,3,4,5 (Box 1). As is often the case, the choice of underlying assumptions can lead to several successful models — some in which honesty of the offspring is the only evolutionarily stable strategy2,3, others where various ‘compromise’ outcomes are possible4,5.

Meanwhile, field biologists have been busy as well and, on page 667 of this issue, Kilner and colleagues 6 describe a two-pronged research programme into honesty and deception among avian nestlings. First, they worked out how the begging signals of nestling reed warblers (Acrocephalus scirpaceus) convey information that seems to be basically honest (at least, as far as the current surrogates of ‘need’ can detect) to the parents. The authors found that warbler chicks increase their gapes and calling rates both as they grow older and as the interval increases since they were last fed. Similarly, chicks that naturally show large gapes and high calling rates consume more food than their less enthusiastic siblings when allowed all the food they want. I leave the reader to make the crucial — and extremely difficult — step of accepting gluttony as a legitimate measure of physiological (much less evolutionary) need. But there is no indication that reed warbler nestlings rip off their parents7,8. Perhaps they are limited by the costliness of their displays, as predicted by honest-signal theory2,3,9. Alternatively, maybe the gap between the evolutionary interests of the parents and offspring is trivial, or even non-existent5,7,8,10.

The second research prong, though, blows away all nuance. When the parent is a reed warbler and the offspring is a common cuckoo chick (Cuculus canorus) whose mother inserted its egg (thoughtfully pre-warmed in her oviduct for an extra day to accelerate hatching) into the warbler nest, all congruencies of Darwinian fitness are out of the window — this is war! The cuckoo hatchling evicts its nest-mates, hatched or otherwise, then accepts all the food that the two warbler parents deliver while growing into a grotesque behemoth11 (Fig. 1). Kilner et al.6 now show that cuckoos produce a begging signal that evades the parent warblers' radar. This signal fits overwhelmingly with what the warblers want to hear, if only imperfectly with what they want to see.

Figure 1: Feed me now! — Cuckoo chick and its reed warbler ‘parent’.
figure1

CORBIS/ROGER TIDMAN

Kilner et al.6 have shown that reed warblers use a combination of visual and vocal signals to work out how much food to bring to the brood. An invading cuckoo chick can fool the reed warblers into feeding it because, although its gape is not as large as that of a brood of warbler chicks, it makes as much noise as up to eight little warblers.

Nestling reed warblers offer two relevant signal components, one visual (the gape area of the entire brood) and one vocal (a chorus of ‘ si⃛si⃛si⃛si ’ calls). These operate more or less independently, and account for different components of the total variance in parental deliveries. The tandem of signals conveys more accurate information about offspring condition than either could alone, so the display is legitimately considered a ‘multiple’ signal9. Parent warblers must have some mental trick for integrating these signal components and adjusting how much effort they put into feeding their brood. For human readers, the ‘simple behavioural rule’ of parent warblers is rendered as a regression equation that accounts for an impressive 62.7% of the variance in parental response.

Faced with this plethora of warbler parent predilections, the cuckoo chick has a serious problem that it must solve. Despite its gargantuan size it has a relatively small beak, so it cannot match the visual stimulus of four gaping warbler nestlings. But Kilner et al.6 have found that warbler parents are sensitive to an array of visual and vocal signal combinations . This leaves room for a bit of bait-and-switch, wherein understatement in one sensory signal can be made up by overstatement in another. So, the cuckoo's beak deficiency is compensated for by vocal wizardry that not only matches the total calling rate of four warbler nestlings (at the age of one week), but rises so fast as the cuckoo grows that it soon sounds like eight little warblers! Interestingly, the total stimulus package — the voice of eight chicks combined with the gape of roughly two — inspires parents to their normal work ethic, and they bring enough food for four warbler chicks to the single interloper. By establishing that warbler parents use the same integration rule when dealing with true offspring and cuckoos alike, Kilner et al. solved a long-standing ethological puzzle over why nestling cuckoos have such extraordinary calls. Of course, the deficiency in the visual signal was caused by the cuckoo's habit of throwing out the host young in the first place, presumably opting for sole access to the delivered food in lieu of retaining some help with the signalling problem.

But why does the cuckoo stop there? Why not hustle the expendable warbler parents into delivering food for five, six or seven? With no shared genetic interests, why not drive them into an early grave? Kilner et al. suggest two good reasons. First, the cuckoo needs its ‘parents’ for ten days more than the warbler offspring would have needed them, so there may be an advantage in allowing the parents to pace themselves and work at a normal level. According to this view, greed and pragmatism are in balance. Alternatively, the cuckoo may have hit a ceiling and, if it cannot sing more rapidly or gape more widely, perhaps it cannot exploit the warbler parents further. For that matter, perhaps the cuckoo chick already gets as much food as it can process — a point that might easily be checked by seeing whether cuckoos of the same species raised by different hosts grow faster in the nests of rapidly delivering hosts and more slowly in meaner circumstances.

So it is that, in the evolutionary arms race between warbler and cuckoo, the parasite has decoded the host's integration rule, adapting what it can offer to cover what it cannot. This phenomenon of pandering to pre-existing sensitivities is known in other contexts, ranging from sexual signals in mites, fishes and frogs12 to faux sexual signals in Homo sapiens (toupees, breast implants, elevator shoes and codpieces). In the cuckoo -host system, it also raises a wonderful question about specificity. Common cuckoos parasitize many species of songbird — some of them apparently for millennia, such that the cuckoo has evolved extraordinary egg mimicry. So, can we expect to see similar communication adaptations in sub-populations of cuckoos that parasitize particular hosts for the multiple-signal integration rules of each host?

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Mock, D. Driving parents cuckoo. Nature 397, 647–648 (1999). https://doi.org/10.1038/17679

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