Social learning of a brood parasite by its host

Arms races between brood parasites and their hosts provide model systems for studying the evolutionary repercussions of species interactions. However, how naive hosts identify brood parasites as enemies remains poorly understood, despite its ecological and evolutionary significance. Here, we investigate whether young, cuckoo-naive superb fairy-wrens, Malurus cyaneus, can learn to recognize cuckoos as a threat through social transmission of information. Naive individuals were initially unresponsive to a cuckoo specimen, but after observing conspecifics mob a cuckoo, they made more whining and mobbing alarm calls, and spent more time physically mobbing the cuckoo. This is the first direct evidence that naive hosts can learn to identify brood parasites as enemies via social learning.     

Visual mimicry of host nestlings by cuckoos

Coevolution between antagonistic species has produced instances of exquisite mimicry. Among brood-parasitic cuckoos, host defences have driven the evolution of mimetic eggs, but the evolutionary arms race was believed to be constrained from progressing to the chick stage, with cuckoo nestlings generally looking unlike host young. However, recent studies on bronze-cuckoos have confounded theoretical expectations by demonstrating cuckoo nestling rejection by hosts. Coevolutionary theory predicts reciprocal selection for visual mimicry of host young by cuckoos, although this has not been demonstrated previously. Here we show that, in the eyes of hosts, nestlings of three bronze-cuckoo species are striking visual mimics of the young of their morphologically diverse hosts, providing the first evidence that coevolution can select for visual mimicry of hosts in cuckoo chicks. Bronze-cuckoos resemble their own hosts more closely than other host species, but the accuracy of mimicry varies according to the diversity of hosts they exploit.     

Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo

Brood parasitism in birds is one of the best examples of coevolutionary interactions in vertebrates. Coevolution between hosts and parasites is assumed to occur because the parasite imposes strong selection pressures on its hosts, reducing their fitness and thereby favouring counter-adaptations (e.g. egg rejection) which, in turn, select for parasite resistance (e.g. egg mimicry). Great spotted cuckoos ( Clamator glandarius ) are usually considered a brood parasite with eggs almost perfectly mimicking those of their host, the magpie ( Pica pica ). However, Cl. glandarius also exploits South African hosts with very different eggs, both in colour and size, while the Cl. glandarius eggs are similar to those laid in nests of European hosts. Here, we used spectrophotometric techniques for the first time to quantify mimicry of parasitic eggs for eight different host species. We found: (1) non-significant differences in appearance of Cl. glandarius eggs laid in nests of different host species, although eggs laid in South Africa and Europe differed significantly; (2) contrary to the general assumption that Cl. glandarius eggs better mimic those of the main host in Europe ( P. pica ), Cl. glandarius eggs more closely resembled those of the azure-winged magpie ( Cyanopica cyana ), a potential host in which there is no evidence of recent parasitism; (3) the appearance of Cl. glandarius eggs was not significantly related to the appearance of host eggs. We discuss three possible reasons why Cl. glandarius eggs resemble eggs of some of their hosts. We suggest that colouration of Cl. glandarius eggs is an apomorphic trait, and that variation between eggs laid in South African and European host nests is due to genetic isolation among these populations and not due to variation in colouration of host eggs.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 551–563.     

How is host egg mimicry maintained in the cuckoo (Cuculus canorus)?

To investigate the evolutionary mechanism (host specificity vs. random searching) maintaining mimicry between cuckoo egg appearance and that of different European cuckoo Cuculus canorus hosts, we studied the level of mimicry between the appearance of C. canorus eggs and that of their hosts' eggs in different habitats in southern Finland by using ultraviolet-visible reflectance spectrophotometry. In the main habitat used by C. canorus for reproduction, eggs laid in nests of different host species differed in appearance. Host use by C. canorus was not related to the abundance of hosts, and the level of mimicry was not related to host abundance in the habitat. Furthermore, a close match between C. canorus egg appearance and that of host eggs within habitats was detected after removing the potentially confounding effect of host abundance. In the only two suitable host species nesting in trees (namely chaffinch Fringilla coelebs and brambling Fringilla montifringilla ) we detected changes in C. canorus egg appearance that paralleled those of the two host species. Thus our findings suggest the existence of a correlation between the appearance of C. canorus eggs and that of their hosts' eggs within different habitat types, and suggest that mimicry is maintained by strict host preferences by each C. canorus female when laying.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 57–68.     

Reconciling genetic expectations from host specificity with historical population dynamics in an avian brood parasite, Horsfield's Bronze-Cuckoo Chalcites basalis of Australia

Mitochondrial DNA (mtDNA) is being used increasingly to explore the evolution of host specificity in avian brood parasites. A stable coevolutionary equilibrium between multiple phylogenetically unrelated hosts and a brood parasitic species predicts that mtDNA diversity in the parasite should be relatively deep and phylogenetically structured. Also, the different intraspecific clades resulting from parasitism to multiple sympatric hosts should themselves occur sympatrically. However, mtDNA diversity in brood parasites is as susceptible to effects of historical population dynamics as in any species. We demonstrate the relevance of these dynamics to the use of mtDNA in understanding coevolution between an Australian brood-parasite, Horsfield's Bronze-Cuckoo Chalcites basalis and its hosts, Malurus fairy-wrens and Acanthiza thornbills. Previous ecological and behavioural analyses argue that Malurus- and Acanthiza-specific host races exist in C. basalis. Yet mtDNA diversity in C. basalis is low and phylogenetically unstructured (mean sequence divergence 0.15 +/- 0.07%, range 0.00%-0.31%) and tests of mtDNA neutrality and range expansion vs. population stability (Tajima's D, Fu & Li's F* and D*, Fu's F(S), mismatch analyses) all indicate that C. basalis has expanded its range very recently, probably within the last few tens of thousands of years following climatic amelioration after a peak of aridity in the late Pleistocene. The low mtDNA diversity and its lack of phylogenetic structure in C. basalis deny the existence of evolutionarily long-term stable host races in C. basalis but not the possibility of recently evolved ones. They highlight the need for renewed behavioural and ecological study of the relationship between C. basalis and its hosts. Our findings illustrate the need to understand the evolutionary context in which a brood parasite and its hosts have evolved if mtDNA data are to be used in testing hypotheses concerning the origin and maintenance of host specificity. They also add to the growing body of work illustrating the use of mismatch analyses and Fu's F(S) in detecting range expansions.     

Avian vision and the evolution of egg color mimicry in the common cuckoo

Coevolutionary arms races are a potent force in evolution, and brood parasite-host dynamics provide classical examples. Different host-races of the common cuckoo, Cuculus canorus, lay eggs in the nests of other species, leaving all parental care to hosts. Cuckoo eggs often (but not always) appear to match remarkably the color and pattern of host eggs, thus reducing detection by hosts. However, most studies of egg mimicry focus on human assessments or reflectance spectra, which fail to account for avian vision. Here, we use discrimination and tetrachromatic color space modeling of bird vision to quantify egg background and spot color mimicry in the common cuckoo and 11 of its principal hosts, and we relate this to egg rejection by different hosts. Egg background color and luminance are strongly mimicked by most cuckoo host-races, and mimicry is better when hosts show strong rejection. We introduce a novel measure of color mimicry-"color overlap"-and show that cuckoo and host background colors increasingly overlap in avian color space as hosts exhibit stronger rejection. Finally, cuckoos with better background color mimicry also have better pattern mimicry. Our findings reveal new information about egg mimicry that would be impossible to derive by the human eye.     

Persistence of host defence behaviour in the absence of avian brood parasitism

The fate of host defensive behaviour in the absence of selection from brood parasitism is critical to long-term host-parasite coevolution. We investigated whether New World Bohemian waxwings Bombycilla garrulus that are allopatric from brown-headed cowbird Molothrus ater and common cuckoo Cuculus canorus parasitism have retained egg rejection behaviour. We found that egg rejection was expressed by 100 per cent of Bohemian waxwings. Our phylogeny revealed that Bohemian and Japanese waxwings Bombycilla japonica were sister taxa, and this clade was sister to the cedar waxwing Bombycilla cedrorum. In addition, there was support for a split between Old and New World Bohemian waxwings. Our molecular clock estimates suggest that egg rejection may have been retained for 2.8-3.0 Myr since New World Bohemian waxwings inherited it from their common ancestor with the rejecter cedar waxwings. These results support the 'single trajectory' model of host-brood parasite coevolution that once hosts evolve defences, they are retained, forcing parasites to become more specialized over time.     

The evolution of egg rejection by cuckoo hosts in Australia and Europe

Exploitation of hosts by brood parasitic cuckoos is expectedto 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 defenses is that thelife-history strategies of some hosts reduce the cost of parasitismto the extent that accepting parasitic eggs in the nest is evolutionarilystable. Under this hypothesis, it pays hosts to accept cuckooeggs if (1) the energetic cost of raising the cuckoo is low,(2) there is time to renest, and (3) clutch size is small. Weparasitized the nests of host and nonhost species with nonmimeticmodel eggs to test whether the evolution of egg recognitionby cuckoo hosts could be explained by life-history variablesof the host. The most significant factor explaining rates ofrejection of model eggs was whether or not a species was a cuckoohost, with hosts rejecting model eggs at a higher rate thannonhosts. Egg-rejection rates were also explained by visibilitywithin the nest and by cuckoo mass. We found little supportfor the life-history model of egg rejection. Our results suggestthat parasitism is always sufficiently costly to select forhost defenses and that the evolution of defenses may be limitedby proximate constraints such as visibility within the nest.     

Brood parasitism selects for no defence in a cuckoo host

In coevolutionary arms races, like between cuckoos and their hosts, it is easy to understand why the host is under selection favouring anti-parasitism behaviour, such as egg rejection, which can lead to parasites evolving remarkable adaptations to ‘trick’ their host, such as mimetic eggs. But what about cases where the cuckoo egg is not mimetic and where the host does not act against it? Classically, such apparently non-adaptive behaviour is put down to evolutionary lag: given enough time, egg mimicry and parasite avoidance strategies will evolve. An alternative is that absence of egg mimicry and of anti-parasite behaviour is stable. Such stability is at first sight highly paradoxical. I show, using both field and experimental data to parametrize a simulation model, that the absence of defence behaviour by Cape bulbuls (Pycnonotus capensis) against parasitic eggs of the Jacobin cuckoo (Clamator jacobinus) is optimal behaviour. The cuckoo has evolved massive eggs (double the size of bulbul eggs) with thick shells, making it very hard or impossible for the host to eject the cuckoo egg. The host could still avoid brood parasitism by nest desertion. However, higher predation and parasitism risks later in the season makes desertion more costly than accepting the cuckoo egg, a strategy aided by the fact that many cuckoo eggs are incorrectly timed, so do not hatch in time and hence do not reduce host fitness to zero. Selection will therefore prevent the continuation of any coevolutionary arms race. Non-mimetic eggs and absence of defence strategies against cuckoo eggs will be the stable, if at first sight paradoxical, result.     

Sheep in wolf's clothing: host nestling vocalizations resemble their cowbird competitor's

Nestlings of many avian brood parasites are virtuosos at mimicking host nestling vocalizations, which, like egg mimicry, presumably ensures acceptance by host parents. Having been accepted, parasitic nestlings then often exaggerate the aspects of the host's display to increase parental care. Host nestlings may, in turn, exaggerate their vocalizations to keep up with the parasite, though this possibility has not been evaluated. We experimentally parasitized song sparrow (Melospiza melodia) nests with a brown-headed cowbird (Molothrus ater) chick to evaluate how host nestlings respond. Vocalizations emitted from experimentally parasitized nests were higher in frequency, and louder, than those from unparasitized nests, consistent with the cowbird exaggerating its signalling. In response, host nestlings exaggerated the frequency and amplitude of their vocalizations, such that they resembled the cowbird's while they 'scaled back' on calls per parental provisioning bout. Sparrows in parasitized nests were fed equally often as sparrows in unparasitized nests, suggesting that exaggerating some aspects of vocalization while scaling back on others can help host nestlings confronted with a cowbird. Our results support the recently proposed hypothesis that signalling in parasitized nests involves a dynamic interaction between parasitic and host nestlings, rather than a one-way process of mimicry by the parasite.     

Egg colour mimicry in the common cuckoo Cuculus canorus as revealed by modelling host retinal function

Some parasite cuckoo species lay eggs that, to the human eye, appear to mimic the appearance of the eggs of their favourite hosts, which hinders discrimination and removal of their eggs by host species. Hitherto, perception of cuckoo-host egg mimicry has been estimated based on human vision or spectrophotometry, which does not account for what the receivers' eye (i.e. hosts) actually discriminates. Using a discrimination model approach that reproduces host retinal functioning, and museum egg collections collected in the south of Finland, where at least six different races of the European cuckoo (Cuculus canorus) coexist, I first assess whether the colour design of cuckoo eggs of different races maximizes matching for two favourite avian hosts, viz. the redstart (Phoenicurus phoenicurus) and the pied wagtail (Motacilla alba). Second, I assess the role of nest luminosity on host perception of mimicry by the same two hosts. Phoenicurus-cuckoo eggs showed a better chromatic matching with the redstart-host eggs than other cuckoo races, and in most cases can not be discriminated. Sylvia-cuckoo eggs, however, showed better achromatic matching with redstart-host eggs than Phoenicurus-cuckoo eggs. Also, Motacilla-cuckoo eggs showed poorer chromatic and achromatic matching with pied wagtail-host eggs than Sylvia-cuckoo eggs. Nest luminosity affected chromatic and achromatic differences between cuckoo and host eggs, although only minimally affected the proportion of cuckoo eggs discriminated by chromatic signals. These results reveal that cuckoo races as assessed by humans do not entirely match with host perception of matching and that achromatic mechanisms could play a main role in the discrimination of cuckoo eggs at low-light levels.     

Evidence for aggressive mimicry in an adult brood parasitic bird,and generalized defences in its host

Mimicry of a harmless model (aggressive mimicry) is used by egg, chick and fledgling brood parasites that resemble the host''s own eggs, chicks and fledglings. However, aggressive mimicry may also evolve in adult brood parasites, to avoid attack from hosts and/or manipulate their perception of parasitism risk. We tested the hypothesis that female cuckoo finches (Anomalospiza imberbis) are aggressive mimics of female Euplectes weavers, such as the harmless, abundant and sympatric southern red bishop (Euplectes orix). We show that female cuckoo finch plumage colour and pattern more closely resembled those of Euplectes weavers (putative models) than Vidua finches (closest relatives); that their tawny-flanked prinia (Prinia subflava) hosts were equally aggressive towards female cuckoo finches and southern red bishops, and more aggressive to both than to their male counterparts; and that prinias were equally likely to reject an egg after seeing a female cuckoo finch or bishop, and more likely to do so than after seeing a male bishop near their nest. This is, to our knowledge, the first quantitative evidence for aggressive mimicry in an adult bird, and suggests that host–parasite coevolution can select for aggressive mimicry by avian brood parasites, and counter-defences by hosts, at all stages of the reproductive cycle.     

Microsatellite loci for population and behavioural studies of Horsfield's bronze‐cuckoo (Chalcites basalis: Aves)

Eight polymorphic microsatellite loci were identified for Horsfield's bronze‐cuckoo (Chalcites basalis). These include seven newly isolated loci from cuckoo genomic libraries enriched for GA and GAAA repeat‐containing clones. These loci have a mean expected heterozygosity of 0.71, a mean number of alleles of 13.8 and a combined exclusion probability (one parent known) of 0.9999. Two loci (Cba01 and Cba07) showed a significant deficiency of heterozygotes and may therefore have null alleles, although this effect could be the result of nonrandom population sampling.     

The impact of learning foster species' song on the evolution of specialist avian brood parasitism

Obligate interspecific avian brood parasites do not build nestsof their own but lay their eggs in the nests of other species.It has been proposed that a flexible song learning mechanism(copying the heterospecific songs of the foster species) facilitatesthe evolution of brood-parasitic behavior. Some sort of songcopying is common to all songbirds; hence, to better understandthe evolution of brood parasitism it is important to study therole of song learning. The proposed hypothesis does not takeinto account that flexible song learning might make mate acquisitionmore difficult because males that are preferred by brood-parasiticfemales would be initially rare. We examine this by means oftwo population dynamic models. By using a recurrence equationmodel of brood parasites competing with their nestbuilding ancestors,we show that flexible song learning is indeed an obstacle tothe evolution of brood parasitism. Results from a more realistic,individual-based model, in which the brood-parasitic trait canevolve more gradually, confirm this finding. However, we alsoshow that the obstacle of flexible song learning can be overcomequite easily when males also are carriers of the brood-parasitictrait. This is probably because brood parasitism is a neutraltrait in males, which increases the number of mutants carryinggenes for brood parasitism, and thus makes the female task offinding suitable partners easier.     

Coevolution between slave-making ants and their hosts: host specificity and geographical variation

We explored the impact of a slave-making ant, Protomognathus americanus, on two of its hosts, Leptothorax longispinosus and L. ambiguus. We showed that, on average, slave-maker colonies conduct raids on 2.7 L. longispinosus and 1.4 L. ambiguus nests in a single year. The more common host, L. longispinosus, survives raiding and colony-founding events in a third of the cases, but the less common host rarely survives attacks from the slave-makers. We compare our results, collected in Vermont, to a study conducted in New York where the slave-maker pressure is much stronger. Our results suggest that in Vermont the slave-maker has a sparing strategy when raiding L. longispinosus, but not when raiding L. ambiguus. Thus coevolution between slave-making ants and their hosts shows host specificity and geographical variation.     

Recognizing odd smells and ejection of brood parasitic eggs. An experimental test in magpies of a novel defensive trait against brood parasitism

One of the most important defensive host traits against brood parasitism is the detection and ejection of parasitic eggs from their nests. Here, we explore the possible role of olfaction in this defensive behaviour. We performed egg‐recognition tests in magpie Pica pica nests with model eggs resembling those of parasitic great spotted cuckoos Clamator glandarius. In one of the experiment, experimental model eggs were exposed to strong or moderate smell of tobacco smoke, whereas those of a third group (control) were cleaned with disinfecting wipes and kept in boxes containing odourless cotton. Results showed that model eggs with strong tobacco scent were more frequently ejected compared with control ones. In another experiment, models were smeared with scents from cloacal wash from magpies (control), cloacal wash or uropygial secretions from cuckoos, or human scents. This experiment resulted in a statistically significant effect of treatment in unparasitized magpie nests in which control model eggs handled by humans were more often rejected. These results provide the first evidence that hosts of brood parasites use their olfactory ability to detect and eject foreign eggs from their nests. These findings may have important consequences for handling procedures of experimental eggs used in egg‐recognition tests, in addition to our understanding of interactions between brood parasites and their hosts.     

Effects of intra- and interspecific brood parasitism on a precocial host, the canvasback, Aythya valisineria

Canvasback ducks (Aythya valisineria) suffer both intra- andinterspecific brood parasitism. During 3 years in Manitoba,80% of canvasback nests (n = 179 nests with completed clutches)were parasitized by redheads (A. americana), other canvasbacks,or both, with an average of 4.7 parasitic eggs per parasitizednest. Parasitism had significant negative effects on the reproductivesuccess of nesting canvasbacks, although the proximate mechanismsinvolved differed from those operating in altricial species.Accidental displacement of eggs when parasitic females forcedtheir way onto host nests was the principal negative effectof parasitism, reducing the number of host eggs that were incubatedand ultimately hatched. Parasitism by redheads was relativelymore costly to canvasbacks than was intraspecific parasitism,with approximately 0.31 and 0.17 host eggs displaced per parasiticredhead and canvasback egg laid, respectively. No additionalnegative effects of parasitism on the hatchability of host eggsoccurred subsequent to parasitic laying. Posthatch survivalof canvasback ducklings was lower in broods from parasitizednests but was unrelated to the presence or absence of redheadducklings. Canvasback hosts resisted intrusions by parasiticfemales but showed no evidence of discrimination against parasiticeggs or ducklings. Because most costs of parasitism in thissystem are inflicted at the time of parasitic laying, subsequentrejection of parasitic eggs or ducklings is probably of littlebenefit to canvasback hosts, while the evolution of behaviorthat might prevent parasitic laying in the first place, suchas more vigorous nest defense, may be constrained by its highcosts     

When caterpillars attack: Biogeography and life history evolution of the Miletinae (Lepidoptera: Lycaenidae)

Of the four most diverse insect orders, Lepidoptera contains remarkably few predatory and parasitic species. Although species with these habits have evolved multiple times in moths and butterflies, they have rarely been associated with diversification. The wholly aphytophagous subfamily Miletinae (Lycaenidae) is an exception, consisting of nearly 190 species distributed primarily throughout the Old World tropics and subtropics. Most miletines eat Hemiptera, although some consume ant brood or are fed by ant trophallaxis. A well‐resolved phylogeny inferred using 4915 bp from seven markers sampled from representatives of all genera and nearly one‐third the described species was used to examine the biogeography and evolution of biotic associations in this group. Biogeographic analyses indicate that Miletinae likely diverged from an African ancestor near the start of the Eocene, and four lineages dispersed between Africa and Asia. Phylogenetic constraint in prey selection is apparent at two levels: related miletine species are more likely to feed on related Hemiptera, and related miletines are more likely to associate with related ants, either directly by eating the ants, or indirectly by eating hemipteran prey that are attended by those ants. These results suggest that adaptations for host ant location by ovipositing female miletines may have been retained from phytophagous ancestors that associated with ants mutualistically.