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Prey are sensitive to even subtle cues of predation risk, which provides the evolutionary potential for parasites to exploit host risk perception. Brood parasitic common cuckoos (Cuculus canorus) lay their eggs in the nests of host species and their secretive laying behaviour enables them to evade host defences. Therefore, it seems paradoxical that female cuckoos often give a conspicuous ‘chuckle’ call after parasitizing a host’s clutch. Here, we show that this hawk-like chuckle call increases the success of parasitism by diverting host parents’ attention away from the clutch and towards their own safety. In our field experiments, reed warbler (Acrocephalus scirpaceus) hosts paid no more attention to the ‘cuck-oo’ call of the male common cuckoo than the call of a harmless dove. However, the chuckle call of the female cuckoo had the same effect as the call of a predatory hawk in distracting the warblers’ attention and reducing rejection of a foreign egg. Our results show that the female cuckoo enhances her success by manipulating a fundamental trade-off in host defences between clutch and self-protection. Female common cuckoos often make a hawk-like call after parasitizing a host’s clutch. Here, field experiments show that this call increases the chances of parasitic success by diverting host parents’ attention.

BACKGROUNDIn December 2019, a novel strain of SARS-CoV-2 emerged in Wuhan, China. Since then, the city of Wuhan has taken unprecedented measures and efforts in response to the outbreak.METHODSWe quantified the effects of control measures on population contact patterns in Wuhan, China, to assess their effects on the progression of the outbreak. We included the latest estimates of epidemic parameters from a transmission model fitted to data on local and internationally exported cases from Wuhan in the age-structured epidemic framework. Further, we looked at the age-distribution of cases. Lastly, we simulated lifting of the control measures by allowing people to return to work in a phased-in way, and looked at the effects of returning to work at different stages of the underlying outbreak.FINDINGSChanges in mixing patterns may have contributed to reducing the number of infections in mid-2020 by 92% (interquartile range: 66–97%). There are benefits to sustaining these measures until April in terms of reducing the height of the peak, overall epidemic size in mid-2020 and probability that a second peak may occur after return to work. However, the modelled effects of social distancing measures vary by the duration of infectiousness and the role school children play in the epidemic.INTERPRETATIONRestrictions on activities in Wuhan, if maintained until April, would likely contribute to the reduction and delay the epidemic size and peak, respectively. However, there are some limitations to the analysis, including large uncertainties around estimates of R0 and the duration of infectiousness.FUNDINGBill and Melinda Gates Foundation, National Institute for Health Research, Wellcome Trust, and Health Data Research UK.

Background: In December 2019, a novel strain of SARS-CoV-2 emerged in Wuhan, China. Since then, the city of Wuhan has taken unprecedented measures and efforts in response to the outbreak. Methods: We quantified the effects of control measures on population contact patterns in Wuhan, China, to assess their effects on the progression of the outbreak. We included the latest estimates of epidemic parameters from a transmission model fitted to data on local and internationally exported cases from Wuhan in the age-structured epidemic framework. Further, we looked at the age-distribution of cases. Lastly, we simulated lifting of the control measures by allowing people to return to work in a phased-in way, and looked at the effects of returning to work at different stages of the underlying outbreak. Findings: Changes in mixing patterns may have contributed to reducing the number of infections in mid-2020 by 92% (interquartile range: 66–97%). There are benefits to sustaining these measures until April in terms of reducing the height of the peak, overall epidemic size in mid-2020 and probability that a second peak may occur after return to work. However, the modelled effects of social distancing measures vary by the duration of infectiousness and the role school children play in the epidemic. Interpretation: Restrictions on activities in Wuhan, if maintained until April, would likely contribute to the reduction and delay the epidemic size and peak, respectively. However, there are some limitations to the analysis, including large uncertainties around estimates of R0 and the duration of infectiousness. Funding: KP, YL, MJ, and PK were funded by the Bill & Melinda Gates Foundation (grant number INV003174), YL and MJ were funded by the National Institute for Health Research (NIHR) (16/137/109), TWR and AJK were funded by the Wellcome Trust (grant number 206250/Z/17/Z), RME was funded by HDR UK (grant number MR/S003975/1), and ND was funded by NIHR (HPRU-2012-10096).This research was partly funded by the National Institute for Health Research (NIHR) (16/137/109) using UK aid from the UK Government to support global health research. The views expressed in this publication are those of the author(s) and not necessarily those of the NIHR or the UK Department of Health and Social Care. We would like to acknowledge (in a randomised order) the other members of the London School of Hygiene & Tropical Medicine COVID-19 modelling group, who contributed to this work: Stefan Flasche, Samuel Clifford, Carl A B Pearson, James D Munday, Sam Abbott, Hamish Gibbs, Alicia Rosello, Billy J Quilty, Thibaut Jombart, Fiona Sun, Charlie Diamond, Amy Gimma, Kevin van Zandvoort, Sebastian Funk, Christopher I Jarvis, W John Edmunds, Nikos I Bosse, and Joel Hellewell. Their funding sources are as follows: Stefan Flasche and Sam Clifford (Sir Henry Dale Fellowship [grant number 208812/Z/17/Z]); Billy J Quilty, Fiona Sun, and Charlie Diamond (NIHR [grant number 16/137/109]); Joel Hellewell, Sam Abbott, James D Munday, and Sebastian Funk (Wellcome Trust [grant number 210758/Z/18/Z] ); Amy Gimma and Christopher I Jarvis (Global Challenges Research Fund [grant number ES/P010873/1]); Hamish Gibbs (Department of Health and Social Care [grant number ITCRZ 03010]); Alicia Rosello (NIHR [grant number PROD-1017-20002]); Thibaut Jombart (RCUK/ESRC [grant number ES/P010873/1], UK PH RST, NIHR HPRU Modelling Methodology); Kevin van Zandvoort (Elrha’s Research for Health in Humanitarian Crises (R2HC) Programme, UK Government (DFID), Wellcome Trust, NIHR). Declaration of Interest: The authors declare no competing interests.

The cation-independent mannose 6-phosphate/insulin-like growth factor-2 receptor (M6P/IGF2R or IGF2R) traffics IGF2 and M6P ligands between pre-lysosomal and extra-cellular compartments. Specific IGF2 and M6P high-affinity binding occurs via domain-11 and domains-3-5-9, respectively. Mammalian maternal Igf2r allele expression exceeds the paternal allele due to imprinting (silencing). Igf2r null-allele maternal transmission results in placenta and heart over-growth and perinatal lethality (>90%) due to raised extra-cellular IGF2 secondary to impaired ligand clearance. It remains unknown if the phenotype is due to either ligand alone, or to both ligands. Here, we evaluate Igf2r specific loss-of-function of the domain-11 IGF2 binding site by replacing isoleucine with alanine in the CD loop (exon 34, I1565A), a mutation also detected in cancers. Igf2rI1565A/+p maternal transmission (heterozygote), resulted in placental and embryonic over-growth with reduced neonatal lethality (80%) observed in homozygotes (Igf2rI1565A/I1565A) suggested that wild-type paternal allele expression attenuates the heterozygote phenotype. To evaluate Igf2r tumour suppressor function, we utilised intestinal adenoma models known to be Igf2 dependent. Bi-allelic Igf2r expression suppressed intestinal adenoma (ApcMin). Igf2rI1565A/+p in a conditional model (Lgr5-Cre, Apcloxp/loxp) resulted in worse survival and increased adenoma proliferation. Growth, survival and intestinal adenoma appear dependent on IGF2R-domain-11 IGF2 binding.

Interactions between avian hosts and brood parasites can provide a model for how animals adapt to a changing world. Reed warbler (Acrocephalus scirpaceus) hosts employ costly defenses to combat parasitism by common cuckoos (Cuculus canorus). During the past three decades cuckoos have declined markedly across England, reducing parasitism at our study site (Wicken Fen) from 24% of reed warbler nests in 1985 to 1% in 2012. Here we show with experiments that host mobbing and egg rejection defenses have tracked this decline in local parasitism risk: the proportion of reed warbler pairs mobbing adult cuckoos (assessed by responses to cuckoo mounts and models) has declined from 90% to 38%, and the proportion rejecting nonmimetic cuckoo eggs (assessed by responses to model eggs) has declined from 61% to 11%. This is despite no change in response to other nest enemies or mimetic model eggs. Individual variation in both defenses is predicted by parasitism risk during the host's egg-laying period. Furthermore, the response of our study population to temporal variation in parasitism risk can also explain spatial variation in egg rejection behavior in other populations across Europe. We suggest that spatial and temporal variation in parasitism risk has led to the evolution of plasticity in reed warbler defenses.

The resemblance of some parasitic cuckoos to Accipiter hawks has been known since an- cient times. Recent experiments show that the hawk-like features of Common Cuckoos (Cuculus canorus) facilitate access to Reed Warbler (Acrocephalus scirpaceus) host nests. However, social infor- mation alerts hosts to see through the cuckoo's mimetic disguise. In turn, this has promoted the evo- lution of a cuckoo polymorphism to thwart host recognition. Here we show by comparative analyses that parasitic cuckoos with hawk-like features (yellow eyes, barred underparts, yellow legs) are more likely to be polymorphic (29% of species) than those without (8% of species). Phylogenetic analyses confirm correlated evolution of hawk-like features and cuckoo polymorphism. We suggest that mim- icry dynamics are particularly likely to promote the evolution of various guises in parasitic cuckoos to beat host defences.

When the risk of encountering enemies varies in space or in time, this may select for plasticity of costly defenses. Hosts are known to vary both mobbing of adult cuckoos and egg rejection with spatiotemporal variation in brood parasitism, but it is unclear what parasitism cues they use to guide their defense plasticity. There is evidence that hosts use cuckoo activity near their nests as a direct cue, but cuckoos are secretive and resemble dangerous birds of prey so hosts may use indirect environmental predictors of parasitism too, such as their nest’s proximity to potential cuckoo lookout perches. Here, we compared reed warbler Acrocephalus scirpaceus nest defense responses with models of various enemies at a parasitized site and at a site where no common cuckoos Cuculus canorus were present. Reed warblers approached model cuckoos less closely and mobbed them less at the unparasitized site. However, at both sites, the warblers reduced their mobbing in a similar manner with increasing distance to the nearest potential cuckoo perch. The variation in response was specific to cuckoos and was not shown to harmless controls. Thus, hosts use both direct (cuckoo presence) and indirect cues (perch distance) of parasitism risk for modulating their costly defenses against their secretive parasite. We suggest that reciprocal selection for detection and suppression of direct and indirect cues provides a unifying feature of cuckoo–host arms races. Key words: brood parasites, coevolution, direct cues, host defense, indirect cues, phenotypic plasticity. [Behav Ecol]

The reciprocal interactions between brood parasites and their hosts provide models for studying coevolution. For example, where hosts have evolved egg or chick discrimination, brood parasites have evolved mimicry of host eggs or chicks. Here, we suggest that there is another form of mimicry by cuckoos. A previous study has shown that naive small birds, with no evolutionary history of brood parasitism, are as afraid of adult common cuckoos Cuculus canorus as of sparrowhawks Accipiter nisus because of their physical resemblance. However, it has yet to be shown whether host species regard cuckoos as hawk like, or how hawk resemblance might benefit the cuckoo. We provide the first evidence that hawk resemblance involving barred underparts is an adaptive brood parasitic trait. We show by plumage manipulations of taxidermic models that reed warbler (Acrocephalus scirpaceus) hosts are more reluctant to approach and mob common cuckoos with barred rather than unbarred underparts. Our results indicate that reed warblers are more aggressive toward cuckoos that appear less hawk like and that hence, hawk resemblance facilitates access to host nests. Therefore, we suggest that cuckoos employ 2 forms of mimicry: To enhance parasitic laying, cuckoo adults are Batesian mimics of hawks, appearing dangerous to adult host survival, when in fact they could be safely attacked. At later stages, cuckoo eggs and chicks are aggressive mimics, appearing harmless but in fact dangerous to host reproduction. These strategies are each countered by host discrimination, providing the means for distinct coevolutionary arms races at successive stages of the host nesting cycle. Key words: brood parasitism, coevolution, cuckoo, dove, mimicry, sparrowhawk. [Behav Ecol]

Previous studies have shown that a female dunnock Prunella modularis increases her reproductive success on average by copulating with more than one male resident on her territory and thereby obtaining extra help in raising offspring. Here we document behavior by females that affects which males copulate with them. During her period of receptivity to copulation, a female in a territory shared by two males often left the dominant (or alpha) male, which guarded her most of the time, and approached the subordinate (or beta) male when he sang. A female's responses to individual males thus tend to increase her own reproductive success by increasing her chances for copulation with both males sharing her territory. Playbacks of tape-recorded songs in the field showed that females approached only songs of resident males, not neighbors. They can therefore discriminate individual males by their songs alone, a capability not previously established for female songbirds. Despite intensive guarding of females by males, mating success among male dunnocks depends in part on female choice.

The cuckoo Cuculus canorus is divided into various gentes, each laying a distinctive egg and favouring a different species as host. It has long been assumed that the gentes remain distinct because female cuckoos lay the same egg-type as their mother and prefer the same host, developing this preference by imprinting on their foster parents. We tested whether imprinting occurred by laboratory experiments with 7 cuckoos originating from reed warbler Acrocephalus scirpaceus nests. Two were transferred soon after hatching to robin Erithacus rubecula nests and were raised by robins, while the other five were raised by reed warblers. When about 12 d old, the nestling cuckoos and their foster parents were transferred from the wild to aviaries, where the fosterers continued to raise the cuckoos to independence. The fosterers were then released and the cuckoos retained and presented, at one and two years of age, with a behavioural choice between robins and reed warblers. None of the cuckoos (five females and two males) displayed a consistent preference for the host that reared them even, in the case of females, after oestradiol implantation. We discuss the inadequacies of our experiment and present data on cuckoo egg types to test whether natal philopatry might be sufficient to maintain the gentes. We suggest that mitochondrial DNA studies, now underway, will help to resolve the issue.

Why some lineages have diversified into larger numbers of species than others is a fundamental but still relatively poorly understood aspect of the evolutionary process. Coevolution has been recognized as a potentially important engine of speciation, but has rarely been tested in a comparative framework. We use a comparative approach based on a complete phylogeny of all living cuckoos to test whether parasite–host coevolution is associated with patterns of cuckoo species richness. There are no clear differences between parental and parasitic cuckoos in the number of species per genus. However, a cladogenesis test shows that brood parasitism is associated with both significantly higher speciation and extinction rates. Furthermore, subspecies diversification rate estimates were over twice as high in parasitic cuckoos as in parental cuckoos. Among parasitic cuckoos, there is marked variation in the severity of the detrimental effects on host fitness; chicks of some cuckoo species are raised alongside the young of the host and others are more virulent, with the cuckoo chick ejecting or killing the eggs/young of the host. We show that cuckoos with a more virulent parasitic strategy have more recognized subspecies. In addition, cuckoo species with more recognized subspecies have more hosts. These results hold after controlling for confounding geographical effects such as range size and isolation in archipelagos. Although the power of our analyses is limited by the fact that brood parasitism evolved independently only three times in cuckoos, our results suggest that coevolutionary arms races with hosts have contributed to higher speciation and extinction rates in parasitic cuckoos.

SummaryCoevolutionary arms races, where adaptations in one party select for counter-adaptations in another and vice versa, are fundamental to interactions between organisms and their predators, pathogens, and parasites [1]. Avian brood parasites and their hosts have emerged as model systems for studying such reciprocal coevolutionary processes [2, 3]. For example, hosts have evolved changes in egg appearance and rejection of foreign eggs in response to brood parasitism from cuckoos, and cuckoos have evolved host-egg mimicry as a counter-response [4–6]. However, the host's front line of defense is protecting the nest from being parasitized in the first place [7–10], yet little is known about the effectiveness of nest defense as an antiparasite adaptation, and its coevolutionary significance remains poorly understood [10]. Here we show first that mobbing of common cuckoos Cuculus canorus by reed warblers Acrocephalus scirpaceus is an effective defense against parasitism. Second, mobbing of cuckoos is a phenotypically plastic trait that is modified strategically according to local parasitism risk. This supports the view that hosts use a “defense in-depth strategy,” with successive flexible lines of defense that coevolve with corresponding offensive lines of the parasite. This highlights the need for more holistic research into the coevolutionary consequences when multiple adaptations and counter-adaptations evolve in concert [11].

Brood parasites and predators pose unique threats that may favour the evolution of enemy-specific defence strategies. We considered whether reed warblers, Acrocephalus scirpaceus, have a specific alarm call for common cuckoos, Cuculus canorus, and whether their alarms attract mates and neighbours. Mounts of cuckoos (threat to nest but harmless to adults) were significantly more likely to be mobbed and were mobbed more strongly, with rasp calls and mandible snaps, than mounts of sparrowhawks, Accipiter nisus (threat to adults only), or teal, Anas crecca (a harmless control). However, calls were not acoustically specific to the kind of enemy presented, but rather varied in usage with mount distance from the nest and mount species. This suggests that reed warbler alarm signals are not functionally referential, but rather convey immediacy of threat to the nest. Mates and neighbours often approached during calling, and playback experiments confirmed they were more likely to be attracted by mobbing calls than by control calls. The response was graded, with higher repetition rates of mobbing calls attracting more individuals. Nevertheless, it is unlikely that mobbing calls functioned solely to attract mates and neighbours because calling continued even after these were attracted and was not more likely when there were close neighbouring nests, and attracted neighbours were sometimes chased away by residents. Our results show that reed warblers discriminate a brood parasite from both a dangerous species and an innocuous species by using graded alarm signals that attract conspecifics. This is compatible with the idea that nest defence by reed warblers includes a specific evolved response to brood parasitism.

The similarity between many Old World parasitic cuckoos (Cuculinae) and Accipiter hawks, in size, shape and plumage, has been noted since ancient times. In particular, hawk-like underpart barring is more prevalent in parasitic than in non-parasitic cuckoos. Cuckoo–hawk resemblance may reflect convergent evolution of cryptic plumage that reduces detection by hosts and prey, or evolved mimicry of hawks by parasitic cuckoos, either for protection against hawk attacks or to facilitate brood parasitism by influencing host behaviour. Here, we provide the first evidence that some small birds respond to common cuckoos Cuculus canorus as if they were sparrowhawks Accipiter nisus . Great tits and blue tits were equally alarmed and reduced attendance at feeders during and after the presentation of mounted specimens of common cuckoos and sparrowhawks, but not in response to control presentations of collared doves or teal. Plumage manipulations revealed that the strong alarm response to cuckoos depended on their resemblance to hawks; cuckoos with barred underparts were treated like hawks, while those with unbarred underparts were treated like doves. However, barring was not the only feature inducing alarm because tits showed similarly strong alarm to barred and unbarred hawks, and little alarm to barred doves. These responses of tits, unsuitable as hosts and hence with no history of cuckoo parasitism, suggest that naive small birds can mistake cuckoos for hawks. Thus, any cuckoo–hawk discrimination by host species is likely to be an evolved response to brood parasitism.

In two years, we provided some female Dunnocks with extra food from January through to July. In one year fed females bred ten days earlier than controls and in another year they bred 22 days earlier, but in neither year did they lay larger clutches. Matched comparisons of the same females on the same territories, who had food in one year but not in the other, showed the same effects. Within both feeder and control females, the earliest breeders were those which had spent more time perching in late winter. Perching time may be a good measure of the time an individual has available above that needed for self maintenance. Therefore females who spent more time perching may have been those first able to cross the threshold of extra time needed for the start of breeding activities.

Reed Warblers Acrocephalus scirpaceus fostering a single nestling Cuckoo Cuculus canorus bring food to it at roughly the same rate as they do to an average-sized brood (three or four) of their own young. The food brought, mostly flies and beetles, is also similar. We conclude that the Cuckoo does not provide a supernormal stimulus. We show that Reed Warblers, given experimentally-enlarged broods of seven or eight, can substantially increase their feeding rate. This raises the question of why the young Cuckoo does not exploit this ‘spare’ feeding capacity of the Reed Warbler hosts. We offer three explanations', (i) that the increased begging necessary would attract predators, (ii) that the young Cuckoo is unable to grow faster, and (iii) that it would not be to the advantage of a young Cuckoo, dependent on its foster parents for about 5 weeks (cf. 3 weeks for Reed Warbler young), to provoke a feeding rate that the warblers could not sustain.

Individuals often vary defences in response to local predation or parasitism risk. But how should they assess threat levels when it pays their enemies to hide? For common cuckoo hosts, assessing parasitism risk is challenging: cuckoo eggs are mimetic and adult cuckoos are secretive and resemble hawks. Here, we show that egg rejection by reed warblers depends on combining personal and social information of local risk. We presented model cuckoos or controls at a pair's own nest (personal information of an intruder) and/or on a neighbouring territory, to which they were attracted by broadcasts of alarm calls (social information). Rejection of an experimental egg was stimulated only when hosts were alerted by both social and personal information of cuckoos. However, pairs that rejected eggs were not more likely to mob a cuckoo. Therefore, while hosts can assess risk from the sight of a cuckoo, a cuckoo cannot gauge if her egg will be accepted from host mobbing. Our results reveal how hosts respond rapidly to local variation in parasitism, and why it pays cuckoos to be secretive, both to avoid alerting their targets and to limit the spread of social information in the local host neighbourhood.

The common cuckoo has several host-specific races, each with a distinctive egg that tends to match its host's eggs. Here, we show that the host-race specializing on reed warblers also has a host-specific nestling adaptation. In playback experiments, the nestling cuckoos responded specifically to the reed warbler's distinctive ‘churr’ alarm (given when a predator is near the nest), by reducing begging calls (likely to betray their location) and by displaying their orange-red gape (a preparation for defence). When reed warbler-cuckoos were cross-fostered and raised by two other regular cuckoo hosts (robins or dunnocks), they did not respond to the different alarms of these new foster-parents. Instead, they retained a specific response to reed warbler alarms but, remarkably, increased both calling and gaping. This suggests innate pre-tuning to reed warbler alarms, but with exposure necessary for development of the normal silent gaping response. By contrast, cuckoo chicks of another host-race specializing on redstarts showed no response to either redstart or reed warbler alarms. If host-races are restricted to female cuckoo lineages, then chick-tuning in reed warbler-cuckoos must be under maternal control. Alternatively, some host-races might be cryptic species, not revealed by the neutral genetic markers studied so far.

Exploitation of hosts by brood parasitic cuckoos is expected to stimulate a coevolutionary arms race of adaptations and counteradaptations. However, some hosts have not evolved defenses against parasitism. One hypothesis to explain a lack of host defensesisthatthelife-historystrategiesof somehostsreducethecost ofparasitism totheextent thatacceptingparasiticeggsinthe nest is evolutionarily stable. Under this hypothesis, it pays hosts to accept cuckoo eggs if (1) the energetic cost of raising the cuckoo is low, (2) there is time to renest, and (3) clutch size is small. We parasitized the nests of host and nonhost species with nonmimetic model eggs to test whether the evolution of egg recognition by cuckoo hosts could be explained by life-history variables of the host. The most significant factor explaining rates of rejection of model eggs was whether or not a species was a cuckoo host, with hosts rejecting model eggs at a higher rate than nonhosts. Egg-rejection rates were also explained by visibility within the nest and by cuckoo mass. We found little support for the life-history model of egg rejection. Our results suggest that parasitism is always sufficiently costly to select for host defenses and that the evolution of defenses may be limited by proximate constraints such as visibility within the nest. Key words: brood parasitism, coevolution, cowbirds, cuckoos, life-history strategies. [Behav Ecol]

Parent birds often give alarm calls when a predator approaches their nest. However, it is not clear whether these alarms function to warn nestlings, nor is it known whether nestling responses are species-specific. The parental alarms of reed warblers, Acrocephalus scirpaceus ("churr"), dunnocks, Prunella modularis ("tseep"), and robins, Erithacus rubecula ("seee") are very different. Playback experiments revealed that nestlings of all three species ceased begging only in response to conspecific alarm calls. These differences between species in response are not simply a product of differences in raising environment, because when newly hatched dunnocks and robins were cross-fostered to nests of the other two species, they did not develop a response to their foster species' alarms. Instead, they still responded specifically to their own species' alarms. However, their response was less strong than that of nestlings raised normally by their own species. We suggest that, as in song development, a neural template enables nestlings to recognize features of their own species' signals from a background of irrelevant sounds, but learning then fine-tunes the response to reduce recognition errors.

We compared genera of nonparasitic cuckoos and two groups of parasitic cuckoos: those raised together with host young ("nonejectors") and those in which the newly hatched cuckoo either ejects the host eggs or chicks, or kills the host young ("ejectors"). Nonejectors are similar to their hosts in body size and parasitize larger hosts than do ejectors, which parasitize hosts much smaller than themselves. In both types of parasite, the cuckoo's egg tends to match the host eggs in size. To achieve this, nonejectors have evolved a smaller egg for their body size than have nonparasitic cuckoos, and ejectors have evolved an even smaller egg. Among ejector cuckoo genera, larger cuckoos have larger eggs relative to the eggs of their hosts, and the relationship between cuckoo egg volume (mass of the newly-hatched cuckoo) and host egg volume (mass to be ejected) did not differ from that predicted by weight-lifting allometry. However, comparing among Cuculus cuckoo species, the allometric slope differed from the predicted, so it is not clear that egg size is related to the need to give the cuckoo chick sufficient strength for ejection. Comparing the two most speciose ejector genera, Chrysococcyx cuckoos (smaller and parasitize dome-nesting hosts) lay eggs more similar in size to their host's eggs than do Cuculus cuckoos (larger and parasitize open cup--nesting hosts). Closer size-matching of host eggs in Chrysococcyx may reflect the following: (1) selection to reduce adult body mass to facilitate entry through small domed nest holes to lay, and (2) less need for a large egg, because longer incubation periods in dome-nesting hosts allow the young cuckoo more time to grow before it need eject host eggs. Copyright 2004.

Previous studies have shown that reed warblers, Acrocephalus scirpaceus , are more likely to reject a cuckoo, Cuculus canorus , egg if they have seen a cuckoo at their nest. This suggests that they would benefit from watching out for cuckoos. We tested whether presentations of a cuckoo mount near the nest (to simulate nest inspection) led to increased nest attendance by the warblers. Cuckoo presentations at completed nests before laying, when males guarded their females closely, led to desertion at 40% of nests before any eggs were laid (there were no desertions after presentations of a jay, Garrulus glandarius , a nest predator). In the remaining cases, there was no effect of the cuckoo on nest attendance before laying began, but a marked increase in male nest attendance (compared with jay and no-presentation controls) on the days the first and second eggs were laid. Cuckoo presentations at the one-egg stage led to the same increase in male nest attendance as did the prelaying presentations. Increased male nest attendance at the one–two-egg stage was not at the expense of mate guarding, because this declined anyway when laying began, and it did not lead to increased paternity loss compared with controls. Overall, 15% of broods had one or two extrapair young (6% of all young extrapair). We conclude that male reed warblers do increase nest guarding in response to cuckoos, but only after their females have begun egg laying, when there are less likely to be costs in lost paternity. Females did not increase nest guarding, perhaps because they need to spend more time foraging during the egg-laying period. Our results suggest that cuckoos should be secretive not only when they lay but also when they monitor host nests beforehand. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Cuckoos (family Cuculidae) show the highest diversity of breeding strategies within one bird family (parental care, facultative and obligate brood parasites). We used independent contrasts from two phylogenies to examine how this variation was related to 13 ecological and life-history variables. The ancestral state was probably tropical, resident, forest cuckoos with parental care. The evolution of brood parasitism was correlated with a shift to more open habitats, a change in diet, increases in species breeding-range size and migration, and a decrease in egg size. Once parasitism had evolved, more elaborate parasitic strategies (more harmful to host fitness) were correlated with decreased egg size, a change in diet, increased breeding-range size and migration, a shortened breeding season and a decrease in local abundance. Establishing the most probable evolutionary pathways, using the method of Pagel, shows that changes in ecological variables (such as migration, range size and diet type) preceded the evolution of brood parasitism, which is likely to be a later adaptation to reduce the cost of reproduction. By contrast, brood parasitism evolved before changes in egg size occurred, indicating that egg size is an adaptive trait in host--parasite coevolution. Our results suggest that the evolution of cuckoo brood parasitism reflects selection from both ecological pressures and host defences.

The common cuckoo Cuculus canorus is divided into host-specific races (gentes). Females of each race lay a distinctive egg type that tends to match the host's eggs, for instance, brown and spotted for meadow pipit hosts or plain blue for redstart hosts. The puzzle is how these gentes remain distinct. Here, we provide genetic evidence that gentes are restricted to female lineages, with cross mating by males maintaining the common cuckoo genetically as one species. We show that there is differentiation between gentes in maternally inherited mitochondrial DNA, but not in microsatellite loci of nuclear DNA. This supports recent behavioural evidence that female, but not male, common cuckoos specialize on a particular host, and is consistent with the possibility that genes affecting cuckoo egg type are located on the female-specific W sex chromosome. Our results also support the ideas that common cuckoos often switched hosts during evolution, and that some gentes may have multiple, independent origins, due to colonization by separate ancestral lineages.

Etude des reactions a l'introduction d'un oeuf de parasites chez deux especes d'Acrocephalus; la premiere, A. arundinaceus, etant l'hote du parasite, cuculus canorus et la seconde A. stentoreus, n'etant pas parasitee. Des modeles differents d'oeufs sont utilises

Davies, N.B. 1999. Cuckoos and cowbirds versus hosts: Co-evolutionary lag and equilibrium. In: Adams, N.J. & Slotow, R.H. (eds) Proc. 22 Int. Ornithol. Congr., Durban. Ostrich 70 (1): 71–79. Experiments show co-evolution between the Common Cuckoo Cuculus canorus and its hosts. Both egg mimicry and laying behaviour of cuckoos have evolved in relation to host defences. In turn, host egg rejection and aggression to cuckoos have evolved in response to parasitism. Selective egg replacement by cuckoos may also lead to egg mimicry but current evidence for this is weak. Hosts incur costs of rejection, so below a critical parasitism frequency they do better to accept. This is reflected in phenotypic flexibility in host defences in relation to small-scale geographical variation and temporal changes in parasitism rate. The puzzle is why so many hosts accept non-mimetic eggs. There are more acceptors among cowbird hosts in North and South America than among cuckoo hosts in Europe or southern Africa, and cowbird hosts...

Nestling birds present vivid gapes and produce loud calls as they solicit food, but the complexity of the display is poorly understood. Here we explain the function of reed warbler begging signals and show how they are exploited by the common cuckoo, Cuculus canorus, a brood parasite. Reed warbler parents integrate visual and vocal signals from their young to adjust their provisioning rates, and the two signals convey more accurate information about offspring need than either does alone. The cuckoo chick has a particularly striking begging display which has been suggested to be irresistible to host parents. However, we show that the cuckoo, reared alone in the nest, presents a deficient visual display, and elicits the same amount of care as a reed warbler brood only by compensating with its exaggerated vocal display. Therefore the cuckoo succeeds not through mimicry of the host brood begging signals, but by tuning into the sensory predispositions of its hosts.

The mouths of begging nestlings vary widely in colour, ranging from yellow in robins, Erithacus rubecula, to red in reed buntings, Emberiza schoeniclus. Two functions have been suggested for bright nestling mouth colour: (1) it may improve the detectability of chicks, particularly in poorly lit nests and (2) within species, it may signal need. We tested these hypotheses in a comparative analysis, measuring the mouth colours of nestlings from 31 species under conditions of standardized light availability and food deprivation. Changes in mouth colour signalled need only among the seed-regurgitating finches. In these species there was a 'red flush' at the onset of begging, which became redder with increasing food deprivation. No other species showed these changes, including the closely related chaffinch, Fringilla coelebs, which feeds its young insects. We found no evidence that mouth colour was correlated with the light available in the nest. We did find, however, that nestlings in darker nests improved their conspicuousness through the relative colour and size of the flange that borders their brightly coloured mouths. Nestlings from darker nests had relatively wider flanges, which were whiter and less densely coloured in relation to their mouth colour, than those of chicks reared in better illuminated nests. Clutch size was not related to mouth or flange colour, or relative flange size. We suggest that nestling mouth colour has not been selected to make chicks detectable, but that this is the function of the surrounding flange. We also discuss reasons why signals of need through mouth colour are not more widespread. Copyright 1998 The Association for the Study of Animal Behaviour.

On Wicken Fen and nearby watercourses eastern England, parasitism by cuckoos, Cuculus canorus, declined from 26% and 16% of reed warbler (Acrocephalus scirpaceus) nests in 1985 and 1986, respectively, to 2 to 6% of nests in 1995 to 1997, owing to a decline in cuckoos. Experiments with model eggs showed that over this 12-year period there was a marked decline in host rejection of non-mimetic eggs, from rejection at 75% of reed warbler nests in 1985 to 1986 to 25%, nests in 1997. Calculations suggest that this decline in host defences is too rapid to reflect only genetic change, and is more likely to be the outcome of adaptive phenotypic flexibility. Two other results show flexibility in host responses. First, there was a seasonal decline in rejection, which accompanied the seasonal decline in parasitism. Second, although rejection did not vary with proximity to a naturally parasitized nest within the 3.4km2 of Wicken Fen and its surrounds, there was no rejection at a small unparasitized population 11km away. Flexible host defences will be advantageous when there are costs of rejection as well as short-term temporal changes and small-scale geographical variation in parasitism rate. Other recent studies reporting changes in host defences may also reflect phenotypic flexibility rather than evolutionary change.

Nestling cuckoos, Cuculus canorus , eject host eggs or young from the nest and are then raised alone by the hosts. Using reed warblers, Acrocephalus scirpaceus , as hosts, we investigated how the single cuckoo chick can command the same provisioning rate as a whole brood of host young. Large size alone is not sufficient to stimulate adequate provisioning because single blackbird, Turdus merula , or song thrush, T. philomelos , chicks of the same mass as a cuckoo were fed at a lower rate. Our experiments show that the key stimulus is the cuckoo chick9s rapid begging call (‘si, si, si, si ...’), which sounds remarkably like a whole brood of host chicks, and which it matched in calling rate. When single blackbird or song thrush chicks were accompanied by loudspeakers that broadcast either cuckoo begging calls or calls of a brood of reed warblers, the hosts increased their provisioning rate to that for a cuckoo chick. We suggest that the cuckoo needs vocal trickery to stimulate adequate care to compensate for the fact that it presents a visual stimulus of just one gape.

In songbirds, males are usually the more competitive sex and they use vocalizations to attract females and to compete with rival males. When levels of female–female competition were experimentally increased in a population of dunnocks,Prunella modularis, females were predicted to increase their vocalization rates and to use vocalizations in comparable ways to competing males. Females produced tseep calls in territorial conflicts with rival females, and trill calls during the pre-breeding and fertile periods when they were left alone by their mate. Males were more likely to approach trills than tseeps, and females were more likely to trill than tseep in response to the song of their mate. Removal experiments to increase polygyny showed that females produced both types of call more when they were competing for male attention. Three out of 13 polygynous, fertile females also produced complex songs when their mate left to join another female. Songs were produced in the same context as the songs of female alpine accentors,P. collaris, a congener which breeds in large, polygynandrous groups where female competition for mates is intense, and females attract males with song. The possible functions of the mate-attracting trills and songs of females are discussed; in dunnocks they may (1) attract mates away from other females to reduce the likelihood of polygyny, (2) ensure that the male copulates sufficiently to cross a helping threshold, and (3) enable the female to assess future levels of parental care from her mate.

Reed warblers sometimes make recognition errors when faced with a mimetic cuckoo egg in their nest and reject one or more of their own eggs rather than the foreign egg. Using the framework of signal detection theory, we analyse responses to model eggs to quantify the costs and benefits of acceptance versus rejection in parasitized and unparasitized nests. We show that below a threshold of 19-41% parasitism, the warblers should accept mimetic cuckoo eggs because the costs of rejection outweigh the benefits, whereas above this threshold they should reject. The warblers behaved as predicted; when they saw a cuckoo at their nest they usually showed rejection, but without the sight of the cuckoo they behaved appropriately for the average parasitism rate in Britain (6%) and tended to accept.

Learning to Recognize a Cuckoo Species that are parasitized by cuckoos have evolved several strategies for trying to avoid having their nests hijacked—one of the most obvious being outright attacking, or mobbing, of cuckoos that enter the area. However, cuckoos are not without evolved defenses—most common cuckoo females look remarkably similar to a small hawk, and this mimicry deters mobbing. Thorogood and Davies (p. 578 ; see the Perspective by Mappes and Lindström ) show that social learning in parasitized birds can thwart this protective mimicry. When hosts observe mimics being mobbed, they are more likely to mob them, themselves, later. However, the hosts will only mob the color morph that they observed being mobbed. This specificity may have allowed for the evolution and maintenance of two female morphs within common cuckoos.

In communally breeding birds the number of helpers at the nest is less when helping depends on shared paternity (cooperative polyandry) rather than on collateral kinship with the brood (helpers are siblings, aunts or uncles). We suggest that this is because a helper's relatedness to the brood decreases with an increasing number of helpers in the first case but not in the second. By using the dunnock, Prunella modularis, as a model system, we investigated why cooperative polyandry in this species rarely involves more than two males by removing females to increase male availability in the population. Females defended by just one male actively solicited matings from a second male who settled on their territory. By contrast, although widowed males also attempted to settle on territories already defended by two males, females usually refused to mate with them even though they had ample opportunity to do so. We show that a female would be unlikely to increase the total parental help she gained by sharing matings between more than two males because of the way males reduce their parental effort in relation to paternity loss, and suggest that mating with more males would also increase sexual harassment. We conclude that female choice may set a limit to cooperative polyandry in birds.

Defeating the Cuckoo Brood parasite-host interactions show ongoing antagonistic coevolution. What mediates rapid behavioral changes that do not reflect genetic change? Davies and Welbergen (p. 1318 ) show that reed warblers learn from their neighbors to behave aggressively toward models of the parasitic common cuckoo. Furthermore, reed warblers seem to be predisposed to learn to respond to cuckoos as enemies: Hosts that witnessed neighbors mobbing a harmless parrot model did not increase their aggression toward a cuckoo model. Thus, birds have templates for threats, and relevant antithreat behaviors can be turned on or off depending on social experience.

When I was a schoolboy, every Sunday I used to go to the local pinewoods and sand dunes to spend the day watching birds. I wrote an account of the species I saw for the school natural history competition and won a book by Niko Tinbergen (1953), ‘The Herring Gull’s World’. (Some time later I discovered that my prize was automatic as mine was the only entry.) Reading this book was a revelation. It revealed to me for the first time a whole new way of asking questions about natural history, a subject which until then I had assumed to consist simply of making species lists. Later, during my undergraduate days, the impression I got was the rather depressing one that you had to be incredibly clever to do research and that new ideas would emerge only from long hours in the laboratory or library. It was refreshing to return to Tinbergen’s book, with its emphasis on patient field observation, which gave the encouraging idea that any birdwatcher could make a great discovery if only he had a spare afternoon and a pair of binoculars.

Sexual dimorphism is ubiquitous in animals and can result from selection pressure on one or both sexes. Sexual selection has become the predominant explanation for the evolution of sexual dimorphism, with strong selection on size-related mating success in males being the most common situation. The cuckoos (family Cuculidae) provide an exceptional case in which both sexes of many species are freed from the burden of parental care but where coevolution between parasitic cuckoos and their hosts also results in intense selection. Here, we show that size and plumage differences between the sexes in parasitic cuckoos are more likely the result of coevolution than sexual selection. While both sexes changed in size as brood parasitism evolved, we find no evidence for selection on males to become larger. Rather, our analysis indicates stronger selection on parasitic females to become smaller, resulting in a shift from dimorphism with larger females in cuckoos with parental care to dimorphism with larger males in parasitic species. In addition, the evolution of brood parasitism was associated with more cryptic plumage in both sexes, but especially in females, a result that contrasts with the strong plumage dimorphism seen in some other parasitic birds. Examination of the three independent origins of brood parasitism suggests that different parasitic cuckoo lineages followed divergent evolutionary pathways to successful brood parasitism. These results argue for the powerful role of parasite–host coevolution in shaping cuckoo life histories in general and sexual dimorphism in particular.

The structure of common cuckoo nestling begging calls differs between the two host-races parasitizing reed warblers (reed warbler-cuckoos) and dunnocks (dunnock-cuckoos; longer syllable duration, lower peak and maximum frequency, narrower bandwidth). Cross-fostering experiments demonstrated that this difference is not genetically fixed but develops through experience. When newly hatched reed warbler-cuckoos were transferred to dunnock nests, they developed begging calls more like those of dunnock-cuckoos, whereas controls transferred to the nests of robins or left to be raised by reed warblers developed calls more typical of reed warbler-cuckoos. We tested the effectiveness of these different calls in stimulating host provisioning by placing in host nests a single blackbird or song thrush nestling (of similar size to a young cuckoo, but lacking its exuberant begging calls); when it begged we broadcast, from a small loudspeaker on the nest rim, recordings of either dunnock-cuckoo or reed warbler-cuckoo begging calls. Playback of dunnock-cuckoo begging calls induced higher levels of provisioning by dunnocks, whereas playback of reed warbler-cuckoo begging calls did so for both reed warblers and robins. We suggest that the young cuckoo (which ejects the host's eggs/chicks and so is raised alone) learns by experience which calls best stimulate host provisioning.

We studied the begging display of nestling cuckoos, Cuculus canorus, reared by reed warbler, Acrocephalus scirpaceus, hosts, to test various hypotheses for the cuckoo's unusually rapid begging call. The hypotheses are not mutually exclusive but focus on different parts of the chain: chick need-begging signals-provisioning by hosts. We reject two hypotheses. (1) Cuckoo chicks do not use their exaggerated begging to counteract host rejection: begging displays varied with hunger and functioned entirely to solicit food. (2) Cuckoos also do not exaggerate their begging calls simply because they need more food than a host brood. Single cuckoos grew at a similar rate to a brood of four reed warblers, and more slowly than a blackbird, Turdus merula, chick (a nonparasitic chick of similar size). Our data support two other hypotheses. (3) To elicit sufficient care in reed warbler nests, the cuckoo must exaggerate the vocal component of its display to compensate for its deficient visual signal (a single gape) compared with a host brood. Thus rapid calling reflects the way the cuckoo exploits the provisioning rules that hosts use to feed their own young. (4) In theory, cuckoos should be more selfish than host young because their greed is unconstrained by kinship. Our data are equivocal; compared with host broods, cuckoos solicited a higher provisioning rate in relation to one measure of need but not for another. We discuss whether cuckoos are likely to have gens-specific begging displays. Copyright 1999 The Association for the Study of Animal Behaviour.

We welcome Soler and Soler's comments1xSoler, M. and Soler, J.J. Trends Ecol. Evol. 1999; 14: 294–295See all References1 on our paper2xKilner, R.M., Noble, D.G., and Davies, N.B. Nature. 1999; 397: 667–672Crossref | Scopus (189)See all References2 in this issue of TREE, and agree that only by understanding both links in the chain: chick need–begging signals–host provisioning3xGodfray, H.C.J. Nature. 1991; 352: 328–330CrossrefSee all References3 can we fully understand cuckoo chick (Cuculus canorus) begging displays. Our Nature paper dealt exclusively with the second link, whereas a forthcoming companion paper4xSee all References4 focuses on the first link.In asserting ‘the cuckoo chick needs the same provisioning rate as an entire brood of reed warblers’ (Acrocephalus scirpaceus), Soler and Soler imply that what the cuckoo chick gets is what it wants. But the two are not necessarily the same4xSee all References4.Turning to the behaviour of cuckoo chicks in other host nests, we agree that it would be fascinating to compare their begging displays. However, predictions cannot easily be made simply from our work on reed warbler hosts. We believe that it is impossible to understand how cuckoo chicks should signal to their host parents without understanding: (1) how the needs of a cuckoo chick compare with those of host young, and (2) how host parents integrate begging signals to determine provisioning rates. There are good reasons for supposing that both will differ between hosts, but precisely how they do remains to be determined.For example, apart from the reed warbler (which weighs ≈12 g), other common British hosts are the dunnock Prunella modularis (≈20 g) and the meadow pipit Anthus pratensis (≈18 g). The larger the host, the more similar the needs of a cuckoo chick and a single host young will be. In a dunnock nest, therefore, a cuckoo might have to call fast enough to compensate for the visual difference between its own gape and that displayed by two to three dunnock nestlings, rather than four nestlings in a reed warbler nest. This assumes, of course, that its optimal growth rate is the same in both nests. However, predictions about the cuckoo's begging displays are further complicated by the fact that the begging call rate of dunnock nestlings is far more rapid than that of reed warbler nestlings (R.M. Kilner and N.B. Davies, unpublished), which might be because dunnock nestlings typically compete with half-sibs rather than full-sibs5xBriskie, J.V., Naugler, C.T., and Leech, S.M. Proc. R. Soc. London Ser. B. 1994; 258: 73–78Crossref | Scopus (110)See all References5. By contrast, meadow pipit young are far less vocal (R.M. Kilner and N.B. Davies, unpublished), perhaps because they occupy ground-nests and so are more vulnerable to predators6xHaskell, D. Proc. R. Soc. London Ser. B. 1994; 257: 161–164CrossrefSee all References6. All of this suggests that cuckoos will have to tune into different offspring–parent communication systems in the nests of different hosts. This presents a fascinating developmental problem, given that cuckoo host races are restricted to the female line7xMarchetti, K., Nakamura, H., and Gibbs, H.L. Science. 1998; 282: 471–472Crossref | PubMed | Scopus (85)See all References7, hinting that either begging is maternally controlled or that cuckoos learn how to beg in different host nests.

It has long been argued that populations of the parasitic common cuckoo Cuculus canorus consist of sympatric host-specific female races, each of which lays eggs that match, to varying degrees, those of their chosen hosts. We tested this hypothesis by comparing rapidly evolving DNA markers among the cuckoo chicks reared by the three most common hosts in the United Kingdom. Comparing cuckoos from different hosts, we found no significant differences in the number of repeats in the control region of the mtDNA nor in the allele frequencies of three microsatellite loci. Given that cuckoos parasitizing the three different hosts do lay different eggs, these results suggest that either: (i) egg-colour variation in cuckoos is facultative, which is unlikely; (ii) gene flow between races occurs because female cuckoos sporadically successfully parasitize alternative hosts; or (iii) the presumably neutral markers in this study have not have not tracked the rapid and/or recent evolution of host races in this species. Studies of the laying and mating patterns of female cuckoos in marked populations in the wild will help evaluate which of these interpretations is most likely.