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.     

The evolution of host specialisation in avian brood parasites

Traditional ecological theory predicts that specialisation can promote speciation; hence, recently derived species are specialists. However, an alternative view is that new species have broad niches, which become narrower and specialised over time. Here, we test these hypotheses using avian brood parasites and three different measures of host specialisation. Brood parasites provide an ideal system in which to investigate the evolution of specialisation, because some exploit more than 40 host species and others specialise on only one. We find that young brood parasite species are smaller and specialise on a narrower range of host sizes, as expected, if specialisation is linked with the generation of new species. Moreover, we show that highly virulent parasites are more specialised, supporting findings in other host–parasite systems. Finally, we demonstrate that different measures of specialisation can lead to different conclusions, and specialisation indices should be designed taking into account the biology of each system.     

Spatial patterns of egg laying and multiple parasitism in a brood parasite: a non-territorial system in the great spotted cuckoo (Clamator glandarius)

We analysed the spatial and temporal pattern of egg laying in great spotted cuckoo females using microsatellite typing to determine parentage of the eggs and nestlings found in host (magpie) nests. The results showed that there were no exclusive laying territories in the study area. Cases of multiparasitism could be due to single females laying two or more eggs in a nest, or to several females using the same nest. In the latter case multiparasitism was due to a shortage of available host nests. We argue that the need for very large laying areas and the likely small cost of sharing parental care for chicks make the costs of defending territories higher than the benefits, which has constrained the evolution of territoriality in this species. Received: 16 March 1998 / Accepted: 15 June 1998     

Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis

A long-term study of the interactions between a brood parasite, the great spotted cuckoo Clamator glandarius, and its primary host the magpie Pica pica, demonstrated local changes in the distribution of both magpies and cuckoos and a rapid increase of rejection of both mimetic and non-mimetic model eggs by the host. In rich areas, magpies improved three of their defensive mechanisms: nest density and breeding synchrony increased dramatically and rejection rate of cuckoo eggs increased more slowly. A stepwise multiple regression analysis showed that parasitism rate decreased as host density increased and cuckoo density decreased. A logistic regression analysis indicated that the probability of changes in magpie nest density in the study plots was significantly affected by the density of magpie nests during the previous year (positively) and the rejection rate of mimetic model eggs (negatively). These results are consistent with a hypothesis (the intermittent arms race hypothesis) of spatially structured cyclic changes in parasitism. During periods of parasitism, host defences continuously improve, and as a consequence, the fitness gains for parasites decrease. When host defences against parasites reach a high level, dispersing parasites have a selective advantage if they are able to emigrate to areas of low resistance. Once parasites have left an area hosts will lose their defensive adaptations due to their cost in the absence of parasitism. The scene is then set for re-colonization by great spotted cuckoos. Received: 7 May 1998 / Accepted: 24 August 1998     

Temporal patterns of host availability, brown-headed cowbird brood parasitism, and parasite egg mass

I studied relationships between temporal patterns of host availability, brood parasitism, and egg mass for the parasitic brown-headed cowbird (Molothrus ater). At a study site consisting largely of edge habitat in north-eastern Illinois, I found 834 bird nests from 27 species. A total of 407 cowbird eggs and nestlings were found in these nests over three laying seasons. Nearly all (n= 379; 93%) were found in the nests of seven host species. For these species and all taken together, weekly nest availability generally decreased whereas parasitism frequency generally increased throughout the cowbird laying season, but the proportions of nests parasitized and the mean number of cowbird eggs in them did not. Additionally, no correlation was found between the proportions of nests parasitized and nest availability. Cowbird egg mass generally increased throughout the laying season, indicating that foraging conditions improved and that, early in the laying season, egg mass and quality may be less important than quantity. Consistently high weekly levels of parasitism indicate that cowbird reproduction was less limited by resources needed for egg production and more by the availability of suitable host nests. Fluctuating weekly host availabilities suggest that previously established, constant rates of cowbird egg laying would produce an excess of eggs during periods of low host availability. Further, the low frequency of parasitism (1%) of nests in stages too advanced for successful parasitism, and of abandoned nests, is consistent with the hypothesis that cowbirds' consistently high rate of egg production helps assure an egg is available when an appropriate nest is found. Frequently, nests were parasitized multiple times, raising the possibility that cowbirds were interfering with their own reproduction. A diverse host community increases the possibility that a decline of any one host species is unlikely to affect cowbird reproduction significantly. Received 11 July 1997 / Accepted: 31 March 1998     

The importance of clutch characteristics and learning for antiparasite adaptations in hosts of avian brood parasites

There is considerable variation in rejection rates of parasitic eggs among hosts of avian brood parasites. In this article, we develop a model that can be used to predict host egg rejection behavior in brood parasite-host systems in general, by considering both intra- and interclutch variation in host egg appearance; clutch characteristics that may be important in calculating the fitness of individuals adopting rejecter or acceptor strategies. In addition, we consider the importance of learning the appearance of own eggs during the first breeding attempt and host probability of survival between breeding seasons on evolution of rejection behavior. Based on this model we can predict at which level of parasitism fitness of rejecter individuals is higher than that of acceptor individuals and vice versa. The model analyses show that variation in egg appearance can be a key factor for the evolution of host defense against parasitism. In more detail, analyses show that we should expect to find a prolonged learning period only in hosts that have a high intraclutch variation in egg appearance, because such hosts may potentially experience high costs in terms of recognition errors. Furthermore, learning is in general more adaptive in parasite-host systems in which hosts do have some reproductive success even when parasitized, and when parasitism rates are moderate. By including variables that have not been considered in previous models, our model represents a useful tool in investigations of host rejection behavior in various host-parasite systems.     

Host nest defense against a color-dimorphic brood parasite: great reed warblers (Acrocephalus arundinaceus) versus common cuckoos (Cuculus canorus)

We tested great reed warbler (Acrocephalus arundinaceus) discrimination against two common cuckoo (Cuculus canorus) female color morphs (gray and rufous) in two areas with different parasitism rates and proportions of the two morphs. Hosts recognized the two cuckoo morphs from a control, the feral pigeon (Columba livia), at Apaj, Hungary (where brood parasitism was heavy), whereas no significant differences among the models were recorded at Lužice, Czech Republic (where the parasitism rate was moderate). At Apaj, the hosts discriminated the rufous morph (which is slightly predominant there) better than the gray morph from the control. Between-site comparison (after controlling for background aggression) revealed that great reed warblers were more aggressive towards the rufous morph at Apaj than at Lužice, whereas their responses to the gray morph did not differ, corresponding with much higher between-site difference in the relative abundance of the rufous morph. Our results suggest that both local parasitism pressure and relative abundance of two female color morphs of a brood parasite may significantly influence host nest defenses.     

A likelihood‐based approach for assessment of extra‐pair paternity and conspecific brood parasitism in natural populations

Genotypes are frequently used to assess alternative reproductive strategies such as extra‐pair paternity and conspecific brood parasitism in wild populations. However, such analyses are vulnerable to genotyping error or molecular artefacts that can bias results. For example, when using multilocus microsatellite data, a mismatch at a single locus, suggesting the offspring was not directly related to its putative parents, can occur quite commonly even when the offspring is truly related. Some recent studies have advocated an ad‐hoc rule that offspring must differ at more than one locus in order to conclude that they are not directly related. While this reduces the frequency with which true offspring are identified as not directly related young, it also introduces bias in the opposite direction, wherein not directly related young are categorized as true offspring. More importantly, it ignores the additional information on allele frequencies which would reduce overall bias. In this study, we present a novel technique for assessing extra‐pair paternity and conspecific brood parasitism using a likelihood‐based approach in a new version of program cervus . We test the suitability of the technique by applying it to a simulated data set and then present an example to demonstrate its influence on the estimation of alternative reproductive strategies.     

Referential alarm calling elicits future vigilance in a host of an avian brood parasite

Yellow warblers (Setophaga petechia) use referential ‘seet’ calls to warn mates of brood parasitic brown-headed cowbirds (Molothrus ater). In response to seet calls during the day, female warblers swiftly move to sit tightly on their nests, which may prevent parasitism by physically blocking female cowbirds from inspecting and laying in the nest. However, cowbirds lay their eggs just prior to sunrise, not during daytime. We experimentally tested whether female warblers, warned by seet calls on one day, extend their anti-parasitic responses into the future by engaging in vigilance at sunrise on the next day, when parasitism may occur. As predicted, daytime seet call playbacks caused female warblers to leave their nests less often on the following morning, relative to playbacks of both their generic anti-predator calls and silent controls. Thus, referential calls do not only convey the identity or the type of threat at present but also elicit vigilance in the future to provide protection from threats during periods of heightened vulnerability.     

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.     

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     

A single ancient origin of brood parasitism in African finches: implications for host-parasite coevolution

Robust phylogenies for brood-parasitic birds, their hosts, and nearest nesting relatives provide the framework to address historical questions about host-parasite coevolution and the origins of parasitic behavior. We tested phylogenetic hypotheses for the two genera of African brood-parasitic finches, Anomalospiza and Vidua, using mitochondrial DNA sequence data from 43 passeriform species. Our analyses strongly support a sister relationship between Vidua and Anomalospiza, leading to the conclusion that obligate brood parasitism evolved only once in African finches rather than twice, as has been the conventional view. In addition, the parasitic finches (Viduidae) are not recently derived from either weavers (Ploceidae) or grassfinches (Estrildidae), but represent a third distinct lineage. Among these three groups, the parasitic finches and estrildids, which includes the hosts of all 19 Vidua species, are sister taxa in all analyses of our full dataset. Many characters shared by Vidua and estrildids, including elaborate mouth markings in nestlings, unusual begging behavior, and immaculate white eggs, can therefore be attributed to common ancestry rather than convergent evolution. The host-specificity of mouth mimicry in Vidua species, however, is clearly the product of subsequent host-parasite coevolution. The lineage leading to Anomalospiza switched to parasitizing more distantly related Old World warblers (Sylviidae) and subsequently lost these characteristics. Substantial sequence divergence between Vidua and Anomalospiza indicates that the origin of parasitic behavior in this clade is ancient (approximately 20 million years ago), a striking contrast to the recent radiation of extant Vidua. We suggest that the parasitic finch lineage has experienced repeated cycles of host colonization, speciation, and extinction through their long history as brood parasites and that extant Vidua species represent only the latest iterations of this process. This dynamic process may account for a significantly faster rate of DNA sequence evolution in parasitic finches as compared to estrildids and other passerines. Our study reduces by one the tally of avian lineages in which obligate brood parasitism has evolved and suggests an origin of parasitism that involved relatively closely related species likely to accept and provide appropriate care to parasitic young. Given the ancient origin of parasitism in African finches, ancestral estrildids must have been parasitized well before the diversification of extant Vidua, suggesting a long history of coevolution between these lineages preceding more recent interactions between specific hosts and parasites.     

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.     

The sight of an adult brood parasite near the nest is an insufficient cue for a honeyguide host to reject foreign eggs

Hosts of brood‐parasitic birds typically evolve anti‐parasitism defences, including mobbing of parasitic intruders at the nest and the ability to recognize and reject foreign eggs from their clutches. The Greater Honeyguide Indicator indicator is a virulent brood parasite that punctures host eggs and kills host young, and accordingly, a common host, the Little Bee‐eater Merops pusillus frequently rejects entire clutches that have been parasitized. We predicted that given the high costs of accidentally rejecting an entire clutch, and that the experimental addition of a foreign egg is insufficient to induce this defence, Bee‐eaters require the sight of an adult parasite near the nest as an additional cue for parasitism before they reject a clutch. We found that many Little Bee‐eater parents mobbed Greater Honeyguide dummies while ignoring barbet control dummies, showing that they recognized them as a threat. Surprisingly, however, neither a dummy Honeyguide nor the presence of a foreign egg, either separately or in combination, was sufficient to stimulate egg rejection.     

Cancer susceptibility and reproductive trade-offs: a model of the evolution of cancer defences

The factors influencing cancer susceptibility and why it varies across species are major open questions in the field of cancer biology. One underexplored source of variation in cancer susceptibility may arise from trade-offs between reproductive competitiveness (e.g. sexually selected traits, earlier reproduction and higher fertility) and cancer defence. We build a model that contrasts the probabilistic onset of cancer with other, extrinsic causes of mortality and use it to predict that intense reproductive competition will lower cancer defences and increase cancer incidence. We explore the trade-off between cancer defences and intraspecific competition across different extrinsic mortality conditions and different levels of trade-off intensity, and find the largest effect of competition on cancer in species where low extrinsic mortality combines with strong trade-offs. In such species, selection to delay cancer and selection to outcompete conspecifics are both strong, and the latter conflicts with the former. We discuss evidence for the assumed trade-off between reproductive competitiveness and cancer susceptibility. Sexually selected traits such as ornaments or large body size require high levels of cell proliferation and appear to be associated with greater cancer susceptibility. Similar associations exist for female traits such as continuous egg-laying in domestic hens and earlier reproductive maturity. Trade-offs between reproduction and cancer defences may be instantiated by a variety of mechanisms, including higher levels of growth factors and hormones, less efficient cell-cycle control and less DNA repair, or simply a larger number of cell divisions (relevant when reproductive success requires large body size or rapid reproductive cycles). These mechanisms can affect intra- and interspecific variation in cancer susceptibility arising from rapid cell proliferation during reproductive maturation, intrasexual competition and reproduction.     

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.     

A generalist brood parasite modifies use of a host in response to reproductive success

Avian obligate brood parasites, which rely solely on hosts to raise their young, should choose the highest quality hosts to maximize reproductive output. Brown-headed cowbirds (Molothrus ater) are extreme host generalists, yet female cowbirds could use information based on past reproductive outcomes to make egg-laying decisions thus minimizing fitness costs associated with parasitizing low-quality hosts. We use a long-term (21 years) nest-box study of a single host, the prothonotary warbler (Protonotaria citrea), to show that local cowbird reproductive success, but not host reproductive success, was positively correlated with the probability of parasitism the following year. Experimental manipulations of cowbird success corroborated that female cowbirds make future decisions about which hosts to use based on information pertaining to past cowbird success, both within and between years. The within-year pattern, in particular, points to local cowbird females selecting hosts based on past reproductive outcomes. This, coupled with high site fidelity of female cowbirds between years, points to information use, rather than cowbird natal returns alone, increasing parasitism rates on highly productive sites between years.     

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.