Egg mimicry by the Pacific koel: mimicry of one host facilitates exploitation of other hosts with similar egg types

When brood parasites exploit multiple host species, egg rejection by hosts may select for the evolution of host‐specific races, where each race mimics a particular host's egg type. However, some brood parasites that exploit multiple hosts with the ability to reject foreign eggs appear to have only a single egg type. In these cases, it is unclear how the parasite egg escapes detection by its hosts. Three possible explanations are: 1) host‐specific races are present, but differences in egg morphology are difficult for the human eye to detect; 2) the brood parasite evolves a single egg type that is intermediate in appearance between the eggs of its hosts; 3) or the parasite evolves mimicry of one of its hosts, which subsequently allows it to exploit other species with similar egg morphology. Here we test these possibilities by quantifying parameters of egg appearance of the brood‐parasitic Pacific koel Eudynamys orientalis and seven of its hosts. Koel eggs laid in the nests of different hosts did not show significant differences in colour or pattern, suggesting that koels have not evolved host‐specific races. Koel eggs were similar in colour, luminance and pattern to the majority of hosts, but were significantly more similar in colour and luminance to one of the major hosts than to two other major hosts, supporting hypothesis 3. Our findings suggest that mimicry of one host can allow a brood parasite to exploit new hosts with similar egg morphologies, which could inhibit the evolution of host defences in naïve hosts.     

Imperfect mimicry of host begging calls by a brood parasitic cuckoo: a cue for nestling rejection by hosts?

Coevolutionary interactions between avian brood parasites and their hosts often lead to the evolution of discrimination and rejection of parasite eggs or chicks by hosts based on visual cues, and the evolution of visual mimicry of host eggs or chicks by brood parasites. Hosts may also base rejection of brood parasite nestlings on vocal cues, which would in turn select for mimicry of host begging calls in brood parasite chicks. In cuckoos that exploit multiple hosts with different begging calls, call structure may be plastic, allowing nestlings to modify their calls to match those of their various hosts, or fixed, in which case we would predict either imperfect mimicry or divergence of the species into host-specific lineages. In our study of the little bronze-cuckoo (LBC) Chalcites minutillus and its primary host, the large-billed gerygone Gerygone magnirostris, we tested whether: (1) hosts use nestling vocalizations as a cue to discriminate cuckoo chicks; (2) cuckoo nestlings mimic the host begging calls throughout the nestling period; and (3) the cuckoo begging calls are plastic, thereby facilitating mimicry of the calls of different hosts. We found that the begging calls of LBCs are most similar to their gerygone hosts shortly after hatching (when rejection by hosts typically occurs) but become less similar as cuckoo chicks get older. Begging call structure may be used as a cue for rejection by hosts, and these results are consistent with gerygone defenses selecting for age-specific vocal mimicry in cuckoo chicks. We found no evidence that LBC begging calls were plastic.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

The costs of avian brood parasitism explain variation in egg rejection behaviour in hosts

Many bird species can reject foreign eggs from their nests. This behaviour is thought to have evolved in response to brood parasites, birds that lay their eggs in the nest of other species. However, not all hosts of brood parasites evict parasitic eggs. In this study, we collate data from egg rejection experiments on 198 species, and perform comparative analyses to understand the conditions under which egg rejection evolves. We found evidence, we believe for the first time in a large-scale comparative analysis, that (i) non-current host species have rejection rates as high as current hosts, (ii) egg rejection is more likely to evolve when the parasite is relatively large compared with its host and (iii) egg rejection is more likely to evolve when the parasite chick evicts all the host eggs from the nest, such as in cuckoos. Our results suggest that the interactions between brood parasites and their hosts have driven the evolution of egg rejection and that variation in the costs inflicted by parasites is fundamental to explaining why only some host species evolve egg rejection.     

Differential reproductive success favours strong host preference in a highly specialized brood parasite

Obligate avian brood parasites show dramatic variation in the degree to which they are host specialists or host generalists. The screaming cowbird Molothrus rufoaxillaris is one of the most specialized brood parasites, using a single host, the bay-winged cowbird (Agelaioides badius) over most of its range. Coevolutionary theory predicts increasing host specificity the longer the parasite interacts with a particular avian community, as hosts evolve defences that the parasite cannot counteract. According to this view, host specificity can be maintained if screaming cowbirds avoid parasitizing potentially suitable hosts that have developed effective defences against parasitic females or eggs. Specialization may also be favoured, even in the absence of host defences, if the parasite's reproductive success in alternative hosts is lower than that in the main host. We experimentally tested these hypotheses using as alternative hosts two suitable but unparasitized species: house wrens (Troglodytes aedon) and chalk-browed mockingbirds (Mimus saturninus). We assessed host defences against parasitic females and eggs, and reproductive success of the parasite in current and alternative hosts. Alternative hosts did not discriminate against screaming cowbird females or eggs. Egg survival and hatching success were similarly high in current and alternative hosts, but the survival of parasitic chicks was significantly lower in alternative hosts. Our results indicate that screaming cowbirds have the potential to colonize novel hosts, but higher reproductive success in the current host may favour host fidelity.     

A game-theoretic model of interspecific brood parasitism with sequential decisions

The interaction between hosts and parasites in bird populations has been studied extensively. This paper uses game-theoretic methods to model this interaction. This has been done in previous papers but has not been studied taking into account the detailed sequential nature of this game. We introduce a model allowing the host and parasite to make a number of decisions which will depend on various natural factors. The sequence of events begins with the host forming a nest and laying a number of eggs, followed by the possibility that a parasite bird will arrive at the nest; if it does it can choose to destroy some of the host eggs and lay one of its own. A sequence of events follows, which is broken down into two key stages; firstly the interaction between the host and the parasite adult, and secondly that between the host and the parasite chick. The final decision involves the host choosing whether to raise or abandon the chicks that are in the nest. There are certain natural parameters and probabilities which are central to these various decisions; in particular the host is generally uncertain whether parasitism has taken place, but can assess the likelihood of parasitism based upon certain cues (e.g. how many eggs remain in its nest). We then use this methodology to model two real-world interactions, that of the Reed Warbler with the Common Cuckoo and also the Yellow Warbler with the Brown-headed Cowbird. These parasites have different methods in the way they parasitize the nests of their hosts, and the hosts can in turn have different reactions to these parasites. Our model predictions generally match the real results well, and the model also makes predictions of the effect of changes in various key parameters on the type of parasitic interactions that should occur.     

Costs to host defence and the persistence of parasitic cuckoos.

Raising genetically unrelated young is maladaptive, yet brood parasitism is widespread in birds. In several systems, hosts can evolve near-perfect defences against the parasite (discrimination and rejection of unlike eggs), making it difficult to understand how the parasite continues to exist. This study demonstrates costs to host defences (e.g. rejection of one's own eggs) such that once the parasite goes extinct on a particular host species, defence mechanisms are selectively disadvantageous. The consequent loss of host defences, and potential for re-exploitation of the host by the parasite, can explain the continued persistence of avian brood parasites. The results provide one general explanation for coexistence of parasites and their hosts.     

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.     

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.     

Combining phylogenetic and ecological information into a new index of host specificity

Host specificity has 2 independent facets: the extent to which different host species are used by a parasite, and the phylogenetic distances among these hosts. Although the number of host species exploited by a parasite commonly is used as a measure of host specificity, it fails to capture ecological and phylogenetic differences among hosts. Here, a new index of host specificity, S(TD)*, is developed and illustrated. This index measures the average taxonomic distinctness among the host species used by a parasite, weighted for the parasite's prevalence in the different hosts. For a given number of host species, the index approaches its minimum value when a parasite achieves high prevalence in a few closely related host species, and the index approaches its highest value when a parasite reaches its highest prevalence values in distantly related host species. Simple hypothetical examples are used to demonstrate the index's computation and some of its properties. The new index is influenced independently both by the taxonomic (or phylogenetic) affinities of a set of host species and by the distribution of prevalence values among these hosts. A single value cannot truly capture all the nuances of a phenomenon as complex as host specificity; nevertheless, the proposed index incorporates the features of specificity that are most relevant to parasitologists and will be a useful tool for comparative studies.     

Discrimination and ejection of eggs and nestlings by the fan-tailed gerygone from New Caledonia

Nestling rejection is a rare type of host defense against brood parasitism compared with egg rejection. Theoretically, host defenses at both egg and nestling stages could be based on similar underlying discrimination mechanisms but, due to the rarity of nestling rejector hosts, few studies have actually tested this hypothesis. We investigated egg and nestling discrimination by the fan-tailed gerygone Gerygone flavolateralis, a host that seemingly accepts nonmimetic eggs of its parasite, the shining bronze-cuckoo Chalcites lucidus, but ejects mimetic parasite nestlings. We introduced artificial eggs or nestlings and foreign gerygone nestlings in gerygone nests and compared begging calls of parasite and host nestlings. We found that the gerygone ejected artificial eggs only if their size was smaller than the parasite or host eggs. Ejection of artificial nestlings did not depend on whether their color matched that of the brood. The frequency of ejection increased during the course of the breeding season mirroring the increase in ejection frequency of parasite nestlings by the host. Cross-fostered gerygone nestlings were frequently ejected when lacking natal down and when introduced in the nest before hatching of the foster brood, but only occasionally when they did not match the color of the foster brood. Begging calls differed significantly between parasite and host nestlings throughout the nestling period. Our results suggest that the fan-tailed gerygone accepts eggs within the size range of gerygone and cuckoo eggs and that nestling discrimination is based on auditory and visual cues other than skin color. This highlights the importance of using a combined approach to study discrimination mechanisms of hosts.     

Egg Recognition and Social Parasitism in Formica Ants

Nests of social insects are an attractive resource in terms of nutrition and shelter and therefore targeted by a variety of pathogens and parasites that harness the resources of a host colony in their own reproductive interests. Colonies of the ants Formica fusca and F. lemani serve as hosts for mound‐building Formica species, the queens of which use host colonies during colony founding. Here, we investigate whether workers of the host species can mitigate the costs imposed on them by invading parasite queens by recognizing and selectively removing eggs laid by these queens. We used behavioural assays, allowing host workers to choose between con‐colonial eggs and eggs laid by the parasite species F. truncorum. We show that workers of both host species discriminate between the two types of eggs in favour of con‐colonial eggs. Moreover, workers of F. fusca rejected more con‐colonial eggs than F. lemani. This higher rate of error in F. fusca may reflect a greater selectivity or a greater difficulty in discriminating between the two egg types. Nevertheless, both host species removed parasite eggs at a similar rate, when these were artificially introduced into the colonies, although some eggs remained after 10 d. In addition, upon receiving parasite eggs, host workers started to lay unfertilized male‐destined eggs within 6 d, thus employing an alternative pathway to gain direct fitness when the resident queen is no longer present and the colony is parasitized.     

Host and brood parasite coevolutionary interactions covary with comparative patterns of the avian visual system

In coevolutionary arms-races, reciprocal ecological interactions and their fitness impacts shape the course of phenotypic evolution. The classic example of avian host–brood parasite interactions selects for host recognition and rejection of increasingly mimetic foreign eggs. An essential component of perceptual mimicry is that parasitic eggs escape detection by host sensory systems, yet there is no direct evidence that the avian visual system covaries with parasitic egg recognition or mimicry. Here, we used eye size measurements collected from preserved museum specimens as a metric of the avian visual system for species involved in host–brood parasite interactions. We discovered that (i) hosts had smaller eyes compared with non-hosts, (ii) parasites had larger eyes compared with hosts before but not after phylogenetic corrections, perhaps owing to the limited number of independent evolutionary origins of obligate brood parasitism, (iii) egg rejection in hosts with non-mimetic parasitic eggs positively correlated with eye size, and (iv) eye size was positively associated with increased avian-perceived host–parasite eggshell similarity. These results imply that both host-use by parasites and anti-parasitic responses by hosts covary with a metric of the visual system across relevant bird species, providing comparative evidence for coevolutionary patterns of host and brood parasite sensory systems.     

Entobdella soleae--pointers to the future

The biology of the monogenean skin parasite Entobdella soleae and its relationship with its host, the common sole (Solea solea), are probably better known than those of any other monogeneans. The author describes his early involvement with this parasite and the special features of parasite and host that make this relationship so suitable for parasitological studies. Aspects of the biology of E. soleae that have been investigated are briefly mentioned, but most of the paper is concerned with areas of the parasite's biology that remain a challenge to determine. Unresolved areas are as follows: (1) the identity of the factor (or factors) in host skin mucus that stimulates hatching of the parasite's eggs; (2) whether or not the larvae of the parasite are attracted to their host; (3) the nature of factors controlling the contrasting behaviour of adult parasites on the upper and lower surfaces of the host; (4) how nutrients are supplied to the remote regions of the haptor; (5) whether the host has any control via its immune system over parasite invasion success and survival; (6) how the parasite copes with the migratory habits of some sole populations, assuming that such populations are infested with the parasite. The intimacy of this parasite/host relationship is its most remarkable feature, the reflection of which, not surprisingly, is the greatly restricted host range of the parasite. E. soleae has been reported from only three host species, all highly specialised bottom-dwelling members of Solea. It is all the more surprising that relatives of E. soleae, such as Neobenedenia melleni, retain the ability to parasitise an enormous range of hosts. How this versatility is achieved remains to be seen.     

Different transmission strategies of a parasite in male and female hosts

We investigated whether a parasite with two routes of transmission responds to the different transmission opportunities offered by male and female hosts by using different transmission strategies in the two sexes. The parasite Ascogregarina culicis, which infects the mosquito Aedes aegypti, can be transmitted as its host’s pupa transforms into an adult or when a female lays its eggs. As the latter transmission route is missing in males, we expected, and found, that the parasite releases a greater proportion of its infectious forms during emergence when it is within a male than when it infects a female. The transmission route, which influences the parasite’s dispersal and the evolution of its virulence, was also affected by the dose of infection and the parasite’s previous transmission route. Our results emphasize the complexity underlying the development of parasites and show their ability to tune their strategy to their environment.     

Nest desertion cannot be considered an egg‐rejection mechanism in a medium‐sized host: an experimental study with the common blackbird Turdus merula

Two main mechanisms of egg rejection, the main defence of hosts against brood parasites, have been described: ejection and desertion. Desertion of the parasitized nest is much more costly and is usually exhibited by small‐sized host species unable to remove the parasitic egg. However, nest desertion is frequently assumed to be an anti‐parasite strategy even in medium or large‐sized host species. This assumption should be considered with caution because: 1) large‐sized hosts able to eject the parasitic egg should eject it rather than desert the nest, and 2) breeding birds may desert their nests in response to different disturbances other than brood parasitism. This problem is especially important in the common blackbird Turdus merula because this is a medium‐sized species, potential host of the common cuckoo Cuculus canorus, in which desertion has been frequently reported as a response to cuckoo egg models. Here, we seek to determine whether nest desertion can be considered a response unequivocally directed to the parasitic egg in medium‐sized hosts using the blackbird as the study species. In an experimental study in which we have manipulated levels of mimicry and size of experimental eggs, we have found that both colour (mimetic and non‐mimetic; at least for human vision) and size (small, medium, and large) significantly affected ejection rates but not nest desertion rates. In fact, although large eggs disproportionally provoked nest desertion more frequently than did small or medium‐sized eggs, cuckoo‐sized parasitic eggs were not deserted allowing us to conclude that desertion is unlikely to be an adaptive response to brood parasitism at least for this species.     

How to analyse host discrimination

Abstract. 1. Two usual definitions of host discrimination are presented. The first is 'the ability of a parasite to distinguish unparasitized from parasitized hosts and to lay eggs in the former'. This definition is not useful and even confusing since it does not include the ability of a parasite to distinguish hosts containing different numbers of parasite eggs and to lay preferably only in those with the lowest numbers.
2. The second definition is 'the ability of a parasite to distribute its eggs in a non-random, regular way among its hosts'. It is argued that most field data are insufficient to permit any conclusions about host discriminative ability on the basis of this definition. An example is given of an apparent random distribution by parasites that are perfectly able to discriminate.
3. Arguments are given for studying the behaviour of the parasite in order to answer the question of host discrimination. Five examples of parasites are presented that would erroneously have been classified as non-discriminators on the basis of the first definition, since they all superparasitize.
4. It is suggested that the meaning of the term 'host discrimination' be extended to include the ability of a parasite to distinguish hosts with different numbers of eggs.     

Body size,trophic level,and the use of fish as transmission routes by parasites

Within food webs, trophically transmitted helminth parasites use predator–prey links for their own transfer from intermediate prey hosts, in which they occur as larval or juvenile stages, to predatory definitive hosts, in which they reach maturity. In large taxa that can be used as intermediate and/or definitive hosts, such as fish, a host species’ position within a trophic network should determine whether its parasite fauna consists mostly of adult or larval helminths, since vulnerability to predation determines an animal’s role in predator–prey links. Using a large database on the helminth parasites of 303 fish species, we tested whether the proportion of parasite species in a host that occur as larval or juvenile stages is best explained by their trophic level or by their body size. Independent of fish phylogeny or habitat, only fish body length emerged as a significant predictor of the proportion of parasites in a host that occur as larval stages from our multivariate analyses. On average, the proportion of larval helminth taxa in fish shorter than 20 cm was twice as high as that for fish over 100 cm in length. This is consistent with the prediction that small fishes, being more vulnerable to predation, make better hosts for larval parasites. However, trophic level and body length are strongly correlated among fish species, and they may have separate though confounded effects on the parasite fauna exploiting a given species. Helminths show varying levels of host specificity toward their intermediate host when the latter is the downstream host involved in trophic transmission toward an upstream definitive host. Given this broad physiological compatibility of many helminths with fish hosts, our results indicate that fish body length, as a proxy for vulnerability to predators, is a better predictor of their use by helminth larvae than their trophic level based on diet content.     

Relationships between parasite abundance and the taxonomic distance among a parasite's host species: an example with fleas parasitic on small mammals

Opportunistic parasite species, capable of exploiting several different host species, do not achieve the same abundance on all these hosts. Parasites achieve maximum abundance on their principal host species, and lower abundances on their auxiliary host species. Taxonomic relatedness between the principal and auxiliary host species may determine what abundance a parasite can achieve on its auxiliary hosts, as relatedness should reflect similarities among host species in ecological, physiological and/or immunological characters. We tested this hypothesis with fleas (Siphonaptera) parasitic on small Holarctic mammals. We determined whether the abundance of a flea in its auxiliary hosts decreases with increasing taxonomic distance of these hosts from the principal host. Using data on 106 flea species from 23 regions, for a total of 194 flea-locality combinations, we found consistent support for this relationship, both within and across regions, and even after controlling for the potentially confounding effect of flea phylogeny. These results are most likely explained by a decrease in the efficiency of the parasite's evasive mechanisms against the host's behavioural and immune defences with increasing taxonomic distance from the principal host. Our findings suggest that host switching over evolutionary time may be severely constrained by the coupling of parasite success with the relatedness between new hosts and the original host.     

The scaling of total parasite biomass with host body mass

The selective pressure exerted by parasites on their hosts will to a large extent be influenced by the abundance or biomass of parasites supported by the hosts. Predicting how much parasite biomass can be supported by host individuals or populations should be straightforward: ultimately, parasite biomass must be controlled by resource supply, which is a direct function of host metabolism. Using comparative data sets on the biomass of metazoan parasites in vertebrate hosts, we determined how parasite biomass scales with host body mass. If the rate at which host resources are converted into parasite biomass is the same as that at which host resources are channelled toward host growth, then on a log-log plot parasite biomass should increase with host mass with a slope of 0.75 when corrected for operating temperature. Average parasite biomass per host scaled with host body mass at a lower rate than expected (across 131 vertebrate species, slope=0.54); this was true independently of phylogenetic influences and also within the major vertebrate groups separately. Since most host individuals in a population harbour a parasite load well below that allowed by their metabolic rate, because of the stochastic nature of infection, it is maximum parasite biomass, and not average biomass, that is predicted to scale with metabolic rate among host species. We found that maximum parasite biomass scaled isometrically (i.e., slope=1) with host body mass. Thus, larger host species can potentially support the same parasite biomass per gram of host tissues as small host species. The relationship found between maximum parasite biomass and host body mass, with its slope greater than 0.75, suggests that parasites are not like host tissues: they are able to appropriate more host resources than expected from metabolically derived host growth rates.