Mimicry vs. similarity: which resemblances between brood parasites and their hosts are mimetic and which are not?

Mimicry is one of the most conspicuous and puzzling phenomena in nature. The best-known examples come from insects and brood parasitic birds. Unfortunately, the term 'mimicry' is used indiscriminately and inconsistently in the brood parasitic literature despite the obvious fact that similarities of eggs, nestlings and adults of brood parasites to their hosts could result from many different processes (phylogenetic constraint, predation, intraspecific arms-races, vocal imitation, exploitation of pre-existing preferences, etc.). In this note I wish to plead for a more careful use of the term. I review various processes leading to a similarity between propagules (both eggs and nestlings) of brood parasites and their hosts and stress that: (1) mimetic and non-mimetic similarities should be differentiated, (2) a mere similarity of host and parasite propagules provides no evidence for mimicry, (3) mimicry is more usefully understood as a (coevolutionary) process rather than an appearance, and (4) mimicry terminology should reflect the process which led to mimetic similarity. Accepting the mimicry hypothesis requires both the experimental approach and rejection of alternative hypotheses explaining similarities of host and parasite propagules.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 69–78.     

Do sex ratio and development differ in sexually size‐dimorphic shiny cowbirds (Molothrus bonariensis) parasitizing smaller and larger hosts?

Two possible patterns of bias in primary sex ratio have been proposed for size‐dimorphic brood parasites that do not evict host chicks: (1) larger males should be laid at greater frequency in hosts larger than the parasite because they compete better (increasing their survival) than females with large host nest‐mates, and (2) more costly males (i.e. the larger sex) should be laid at greater frequency in hosts smaller than the parasite because, in these hosts, parasite nestlings are provisioned at a higher rate and grow faster than in larger hosts. We tested these hypotheses in two hosts of the sexually size‐dimorphic shiny cowbird, Molothrus bonariensis, one smaller (house wren, Troglodytes aedon) and one larger (chalk‐browed mockingbird, Mimus saturninus) than the parasite. We measured: (1) sex ratio at laying; (2) development of sexual differences in body mass during the nestling stage; and (3) chick survival and sex ratio of chicks before fledging. In both hosts, we found sexual differences in body mass of nestlings from 7 days of age onwards, although we did not find a bias in the sex ratio of eggs laid and chicks fledged. The results of the present study do not support the hypothesis that shiny cowbird females benefit from biasing the primary sex ratio depending on the size of the hosts they parasitize. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 442–448.     

Kleptoparasitic interactions throughout the animal kingdom and a re-evaluation, based on participant mobility, of the conditions promoting the evolution of kleptoparasitism

Understanding of the conditions encouraging the evolution of kleptoparasitism has been limited by the preponderance of attention focused on a limited number of taxa (predominantly birds). However, most animal taxa contain kleptoparasitic members. In many ways, adult birds are aberrant because most are acrobatic, capable of three-dimensional movement, and steal from hosts that are capable of similar feats. The mobility of kleptoparasites and their hosts falls along a continuum, with the acrobatic birds at one end and sessile hosts and kleptoparasites at the other. Considering sedentary systems requires amendments to the criteria previously outlined as necessary for kleptoparasitism. Kleptoparasitic interactions between agile participants are ephemeral, involve numerous hosts over the lifetime of the kleptoparasite, and usually rely on vision. Large concentrations of hosts and large, high-quality food items are important in mobile systems. By contrast, the long-term, intimate associations of sedentary interactions demand that the host not consume the kleptoparasite's offspring and that the host must either have a longer life cycle than the kleptoparasite or be located in aggregations that have staggered life cycles (so the kleptoparasite can move to a new host when the original host dies). Expanding studies of kleptoparasitism to other taxa will differentiate between the selective pressures and evolutionary responses that are universal among kleptoparasitic symbioses and those that are restricted to certain groups.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 745–762.     

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.     

Ectoparasites and age-dependent survival in a desert rodent

Host age is one of the key factors in host–parasite relationships as it possibly affects infestation levels, parasite-induced mortality of a host, and parasite distribution among host individuals. We tested two alternative hypotheses about infestation pattern and survival under parasitism in relation to host age. The first hypothesis assumes that parasites are recruited faster than they die and, thus, suggests that adult hosts will show higher infestation levels than juveniles because the former have more time to accumulate parasites. The second hypothesis assumes that parasites die faster than they are recruited and, thus, suggests that adults will show lower infestation levels because of acquired immune response and/or the mortality of heavily infested juveniles and, thus, selection for less infested adults. As the negative effects of parasites on host are often intensity-dependent, we expected that the age-related differences in infestation may be translated to lower or higher survival under parasitism of adults, in the cases of the first and the second hypotheses, respectively. We manipulated ectoparasite numbers using insecticide and assessed the infestation pattern in adult and juvenile gerbils (Gerbillus andersoni) in the Negev Desert. We found only a partial support for age-dependent parasitism. No age-related differences in infestation and distribution among host individuals were found after adjusting the ectoparasite numbers to the host’s surface area. However, age-related differences in survival under parasitism were revealed. The survival probability of parasitized juveniles decreased in about 48% compared to unparasitized hosts while the survival probability of adults was not affected by ectoparasites. Our results suggest that the effect of host age on host–parasite dynamics may not explicitly be determined by age-dependent differences in ectoparasite recruitment or mortality processes but may also be affected by other host-related and parasite-related traits.     

Coevolution of daily activity timing in a host–parasite system

Coevolutionary theories applied in the study of host–parasite systems indicate that lineages exhibit progressive trends in response to reciprocal selective pressures. Avian brood parasites have generated intense interest as models for coevolutionary processes. Similar to avian cuckoos, Polistes wasp social parasites usurp a nest and exploit the parental care of a congeneric species to rear their own brood. In the present study, we show a coevolutionary arms race in the daily activity pattern in a Polistes host–parasite pair. We measured the daily activity rate, in constant laboratory conditions, of both host and parasite females during the period in which nest usurpations occur. The parasites showed a hyperkinesis in the middle of the day. As the field observations suggested, this mid-day activity is used to perform host nest usurpation attempts. Timing the usurpations allows the parasite to maximize its usurpation attempts during daytime when the host defence is lower. A field comparison of host presence on the nest in two populations with different parasitism rates showed that populations under strong parasitic pressure exhibit timing counteradaptations to optimize nest defence. This study provides the first example of a mutual coadaptation in timing activity in a parasite–host system.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 399–405.     

Encounter rate between local populations shapes host selection in complex parasite life cycle

The present study aimed to understand how a parasite with a complex life cycle selects a given host succession when several potential hosts are present. Ligula intestinalis (Cestoda, Pseudophyllidea) was considered, which presents a life cycle with three hosts: copepod, fish, and piscivorous bird. Encounter probability between each pair of hosts was calculated for Lavernose-Lacasse gravel pit (France) using a sum of the product of the host abundances over time. Among four potential copepod hosts, two potential fish hosts, and six potential bird hosts, the results demonstrate that the copepod Eudiaptomus gracilis , the roach ( Rutilus rutilus ), and the great crested grebe ( Podiceps cristatus ) had a maximal encounter probability due to their abundance, but also due to the similarities of the temporal dynamics of their life cycles. These results agree with previous experiments and field work identifying a high specificity of L. intestinalis to E. gracilis , R. rutilus , and P. cristatus in the study site. This suggests that the abundance of potential hosts and the temporal dynamics of their life cycles act together to determine encounter rates between hosts and parasites, and thus could constitute a crucial determinant in local host selection by parasites with a complex life cycle.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 99–106.     

Differences in intestinal microbiota between avian brood parasites and their hosts

The intestinal microbiota determines the effectiveness of digestion in vertebrates, and is influenced by the external environment (mainly the diet), gut characteristics, and phylogeny. Avian brood-parasitic nestlings of the sub-family Cuculinae develop in nests of phylogenetically distant passerines and can be fed with the host diet. If the shaping of bacterial communities is dominated by phylogenetic constraints, and therefore the microbiota of parasitic nestlings differs from that of host nestlings, the energy and micronutrients that parasites and hosts obtain from a similar amount of food would be different. In this case, the bacterial communities of parasitic and host nestlings would have important consequences with respect to brood parasite development. By experimentally creating mixed broods of magpies ( Pica pica ) and great spotted cuckoos ( Clamator glandarius ), we investigated their cloacal microbiota using ribosomal intergenic spacer analysis. We found significant differences in bacterial assemblages of the parasitic and host nestlings, although none of the phylotypes were specific in either great spotted cuckoos or magpies. Cuckoos presented more complex communities, which could help the brood parasitic life style and allow the digestion of food provided by different potential hosts. Moreover, the intestinal morphology is different between the two species due to phylogenetic differences in the two taxa, which would influence the dissimilar bacterial assemblages. The detected differences in microbiota of great spotted cuckoo and magpie nestlings, which might occur in other brood parasite–host systems, may imply a lower digestion efficiency in parasites. Thus, the higher level requirements of cuckoo nestlings may be explained, at least in part, by cuckoos having a suboptimal bacterial community for processing the host diet.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 406–414.     

Variation in stickleback head morphology associated with parasite infection

Parasites can affect host phenotypes, influencing their ecology and evolution. Host morphological changes occurring post-infection might result from pathological by-products of infection, or represent adaptations of hosts or parasites. We investigated the morphology of three-spined sticklebacks, Gasterosteus aculeatus , from a population naturally infected with Schistocephalus solidus , which grows to large sizes in their body cavity. We examined local effects of infection on trunk shape, which are imposed directly by the bulk of the growing parasite, and distant effects on head morphology. We show that trunk shape differed between infection classes, and was affected more severely in fish with heavier total parasite mass. We further show unexpected differences in head morphology. The heads of infected fish were reduced in size and differently shaped to those of non-infected fish, with infected fish having deeper heads. Importantly, both head size and shape were also affected more severely in fish with heavier total parasite mass. This latter result suggests that differences in morphology are caused by post-infection changes. Such changes may be incidental, evolutionarily neutral 'side effects' of infection. However, because head morphology affects foraging ecology, such changes are likely to have fitness consequences for hosts, and may constitute adaptations, either of hosts or of parasites. We discuss our finding in the context of the evolution of phenotypic plasticity, and suggest testable hypotheses examining the proximate mechanisms underlying these morphological effects and their potential evolutionary basis.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 759–768.     

Effects of maternal parasite load on offspring life-history traits in the common lizard (Lacerta vivipara)

We studied the effect of maternal ectoparasite load (measured at parturition) on the life-history traits of the offspring of the host Lacerta vivipara, the European common lizard. The ectoparasite, a mite belonging to the family Laelapidae, had a detrimental effect on its host: parasite load was associated with increased host mortality, and was negatively correlated with host body mass. Parasite load was persistent over time, suggesting that parasite load can be predictable. Offspring of highly parasitised mothers had higher values of several fitness components early in life than offspring of parasite-free mothers or lightly infested mothers. This was expressed in terms of increased F₁ yearling growth rate, and reproductive investment at first reproduction (measured as F₂ hatchling mass). These results are interpreted as a host adaptation to attenuate the impact of parasites. Indeed, if high parasite loads arise from long exposure time to a constant population of parasites, and if the negative effects of parasites are additive over time, hosts could reduce the impact of parasites simply by investing more during the earlier stages of life. Naturally, having better performance early in life should lead to higher mortality rates and/or lower fecundity later in life.     

Begging call matching between a specialist brood parasite and its host: a comparative approach to detect coevolution

Studies of avian brood parasite systems have typically investigated the mimicry of host eggs by specialist parasites. Yet, several examples of similarity between host and parasite chick appearance or begging calls suggest that the escalation of host–parasite arms races may also lead to visual or vocal mimicry at the nestling stage. Despite this, there have been no large-scale comparative studies of begging calls to test whether the similarity of host and parasite is greater than predicted by chance or phylogenetic distance within a geographically distinct species assemblage. Using a survey of the begging calls of all native forest passerines in New Zealand, we show that the begging call of the host-specialist shining cuckoo ( Chrysococcyx lucidus ) is most similar to that of its grey warbler ( Gerygone igata ) host compared to any of the other species, and that this is unlikely to have occurred by chance. Randomization tests revealed that the incorporation of the shining cuckoo's begging calls into our species-set consistently reduced the phylogenetic signal within cluster trees based on begging call similarity. By contrast, the removal of the grey warbler calls did not reduce the phylogenetic signal in the begging call similarity trees. These two results support a scenario in which coevolution of begging calls has not taken place: the begging call of the host retains its phylogenetic signal, whereas that of the parasite has changed to match that of its host.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 208–216.     

Relationship Between Nest Predation Suffered by Hosts and Brown-Headed Cowbird Parasitism: A Comparative Study

There are at least four main hypotheses that may explain how the evolution of host selection by avian brood parasites could be linked to nest predation among their potential hosts. First, selection may have favoured parasite phenotypes discriminating among hosts on the basis of expected nest failure. Second, parasitized nests may be more easily detected by predators and extra costs of parasitism may accelerate the evolution of host defences. Third, selection may have favoured predator phenotypes avoiding parasitized nests because parasitism enhances nest defence. Fourth, female brood parasites may directly or indirectly induce host nesting failures in order to enhance future laying opportunities. We collected data on brood parasitism and nest failure due to predation to test these hypotheses in a comparative approach using North American passerines and their brood parasite, the brown-headed cowbird Molothrus ater. Under the hypotheses 1 or 3 we predicted brood parasitism to be negatively associated with nest predation across species, whereas this relation is expected to be positive if hypotheses 2 or 4 are true. We demonstrate that independent of host suitability, nest location, habitat type, length of the nestling period, body mass and similarity among species due to common ancestry, species experiencing relatively high levels of nest predation suffered lower levels of cowbird parasitism. Our results suggest a previously ignored role for nest predation suffered by hosts on the dynamics of the coevolutionary relationships between hosts and avian brood parasites. Co-ordinating editor: Dr. F. Stuefer     

Pirate ants (Polyergus breviceps) and sympatric hosts (Formica occulta and Formica sp. cf. argentea): host specificity and coevolutionary dynamics

The pace and trajectory of coevolutionary arms races between parasites and their hosts are strongly influenced by the number of interacting species. In environments where a parasite has access to more than one host species, the parasite population may become divided in preference for a particular host. In the present study, we show that individual colonies of the pirate ant Polyergus breviceps differ in host preference during raiding, with each colony specializing on only one of two available Formica host species. Moreover, through genetic analyses, we show that the two hosts differ in their colony genetic structure. Formica occulta colonies were monogynous, whereas Formica  sp. cf. argentea colonies were polygynous and polydomous (colonies occupy multiple nest sites). This difference has important implications for coevolutionary dynamics in this system because raids against individual nests of polydomous colonies have less impact on overall host colony fitness than do attacks on intact colonies. We also used primers that we designed for four microsatellite loci isolated from P. breviceps to verify that colonies of this species, like other pirate ants, are comprised of simple families headed by one singly mated queen.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 565–572.     

Evolution and determinants of host specificity in the genus Lamellodiscus (Monogenea)

The evolution and determinants of host specificity in Lamellodiscus species (Monogenea, Diplectanidae) were investigated. The 20 known Mediterranean species were studied, all parasites of fishes from the family Sparidae (Teleostei). An index of specificity, which takes into account the phylogenetic relationships of their fish host species, was defined. The link between specificity and its potential determinants was investigated in a phylogenetic context using the method of independent contrasts. Host specificity in Lamellodiscus species appeared to be highly constrained by phylogeny, but also linked to host size. Mapping specificity onto the parasite phylogenetic tree suggests that specialist species do not represent an evolutionary dead end, and that specialization is not a derived condition. It is hypothesized that the ability to be generalist or specialist in Lamellodiscus is controlled by intrinsic, phylogenetically-related characteristics, and that specialist species tend to use large hosts, which may be more predictable.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77, 431−443.     

Marked variation in parasite resistance between two wild populations of the Trinidadian guppy, Poecilia reticulata (Pisces: Poeciliidae)

This is the first study to demonstrate significant differences between two natural Trinidadian guppy populations in susceptibility to a pathogenic monogenean parasite, Gyrodactylus turnbulli . Following experimental infection with an isogenic laboratory culture of G. turnbulli , fish from the Upper Aripo (UA) lost parasites more slowly and carried up to three times as many parasites at peak infection than did those from the Lower Aripo (LA). The UA population appeared to be more susceptible than the LA fish, even though fish of both populations were naïve to this particular laboratory strain of G. turnbulli and had not encountered any gyrodactylid infection for at least 65 days. The parasite infection reduced the feeding response and feeding activity of UA and LA fish to a similar extent. Our findings suggest that this ectoparasite may have an important impact on the evolutionary biology of guppies (and possibly of other teleosts), particularly as the prevalence of Gyrodactylus infection in natural populations may be as high as 50%. We discuss the role of parasite infections on natural and sexual selection, the good genes model and the implications for immunogenetics in small genetically isolated host populations.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 645–651.     

Costs and consequences of superparasitism in the polyembryonic parasitoid Copidosoma koehleri (Hymenoptera: Encyrtidae)

Abstract.  1. Polyembryonic wasps provide dramatic examples of intra-specific developmental conflict. In these parasitoids, each egg proliferates into a clonal lineage of genetically identical larvae. If more than one egg is laid in a host (superparasitism), individuals of different clones may compete for food resources.
2. In the polyembryonic encyrtid Copidosoma koehleri , one larva per clone can differentiate into a sterile soldier. It is shown that soldiers are always females, and that they attack intra-specific competitors.
3. Research hypotheses were that (a) clones that develop in superparasitised hosts suffer heavier mortality than clones that develop in singly parasitised hosts, and (b) female clones cause higher mortality to their competitors than male clones, hence larval survival is lower in superparasitised hosts that contain females than in male-only broods.
4. The potential frequency of superparasitism in C. koehleri was manipulated by varying parasitoid–host ratios and exposure durations.
5. As parasitoid densities and exposure durations increased, the frequency of superparasitism rose, brood sizes increased, but the number of hosts that completed development was reduced. The number of offspring per parasitoid female decreased with increasing parasitoid–host ratios. Offspring size and longevity were inversely correlated with brood size. As superparasitism rates increased, fewer all-male broods were produced. Male–female broods were female-biased, suggesting selective killing of males by female soldiers. All-female broods were significantly smaller than all-male broods at high parasitoid densities only, possibly reflecting aggression among soldiers of competing clones.
6. The results support the working hypotheses, and suggest that female larvae outcompete males in superparasitised hosts.     

Influences of parasites and thermoregulation on grouping tendencies in marine iguanas

I determined whether grouping behavior influences parasite loadand body temperature of Galápagos marine iguanas, reptilesthat rest gregariously. Mobile (or predatory) Ornithodoros ticks(4.7 mm average body length) approached at a ground speed of65 cm/min and parasitized sleeping marine iguanas for 3.7 hper night, drawing about 0.1 ml blood. Contagiously transmittedAmblyomma ticks hang on to iguana hosts for days or weeks. Marineiguanas sleeping alone had 2.0 mobile ticks per night, whileindividuals sleeping in groups had 0.1 to 1.1 mobile ticks pernight. Single iguanas decreased their mobile parasite load to0.2 ticks per night by sleeping on bushes. Experimental nightlytranslocation of iguanas to areas without other sleeping iguanassignificantly increased their mobile parasite burden above levelsencountered by naturally single individuals (n = 4.6 ticks pernight). Creating an experimental group of two animals reducedinfestation with mobile ticks by 59% compared to levels on singleanimals. Over the course of weeks, mobile ectoparasite loadsat grouping sites increased to levels found at single sites,at which point marine iguanas changed sleeping sites. Groupinghad no effect on the prevalence of contagious ticks. Furthermore,grouping did not help to conserve body temperature in Genovesaiguanas, as measured by radiotelemetry. I conclude that marineiguanas group during daytime at microhabitats favored for thermoregulation(predation is absent in this population). Thermoregulation wasnot of prime importance for nightly aggregations, which insteadserved to reduce mobile ectoparasite load. As a minimum costof infestation, I estimate that individuals sleeping alone wouldhave a 5.4% lower annual energy budget due to tissue removal,not including potential internal infections.     

Taxonomic relationships between Pachycerus and Rhabdorrhynchus (Coleoptera: Curculionidae: Lixinae), with descriptions of two new species of Rhabdorrhynchus from the Arabian Peninsula

Taxonomic relationships between Rhabdorrhynchus and Pachycerus are discussed, and two new species of Rhabdorrhynchus are described: Rhabdorrhynchus sauditus (type locality: Saudi Arabia, As Shāqqah al Yamānīyah, 19°42'N, 40°48'E) and Rhabdorrhynchus emir (type locality: United Arab Emirates, Jebel Ali, 24°59'N, 55°43'E). Some hypotheses on the distribution of the new species in the Arabian Peninsula, based on a biogeographical analysis, are proposed.  © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society , 2008, 152 , 25–37.     

The effect of Jacobin Cuckoo Clamator jacobinus parasitism on the body mass and survival of young in a new host species

The southern African subspecies of Jacobin Cuckoo Clamator jacobinus serratus is a brood parasite of a range of host species. While Jacobin Cuckoos do not evict host young, previous research has found that host young rarely survive the nestling period. Here we provide the first records of Jacobin Cuckoo parasitism of a new host species, the Southern Pied Babbler Turdoides bicolor. We investigate rates of brood parasitism and the survival of host young. The Southern Pied Babbler is one of the largest recorded hosts for Jacobin Cuckoos and, unusually, we find that host young tend to survive the nestling period and maintain similar body mass to host young in unparasitized broods. However, host young were less likely to survive to independence than young raised in unparasitized nests, suggesting a post‐fledging reproductive cost to hosts.     

Adaptations in the common cuckoo (Cuculus canorus) to host eggs in a multiple-hosts system of brood parasitism

The common cuckoo Cuculus canorus parasitism greatly reduces the reproductive success of its hosts and imposes strong selection pressure for hosts to evolve defences against parasitism, such as the ability to recognize and reject dissimilar parasitic eggs, which, in turn, selects for better egg mimicry by the cuckoo. In the co-evolutionary interaction, however, it remains unknown how the cuckoo successfully expanded its range of host usage and how they developed egg mimicry. Most previous studies were conducted in areas where a very few number of host species (i.e. one or two at most) are sympatric with the cuckoo. Several host species, however, breed sympatric with the cuckoo and have been parasitized in the study site in Nagano, central Japan. Such a multiple-hosts system will provide valuable insights for understanding the cuckoo–hosts interactions in the past. In the present study, we report quantitative profiles of eggs based on spectrometer reflectance for four major host species and the corresponding cuckoo gentes. The hosts include the oriental reed warbler ( Acrocephalus orientalis ), bull-headed shrike ( Lanius bucephalus ), azure-winged magpie ( Cyanopica cyana ), and black-faced bunting ( Emberiza spodocephala ). We show that (1) egg morphs of each host and corresponding cuckoo gens can be categorized by two chromatic components of reflectance spectra and (2) there is a significant difference in a particular chroma component between hosts and the cuckoo. We suggest that the cuckoo parasitism in central Japan originated from parasitism on the black-faced bunting.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 291–300.