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

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

The evolution of 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 modelling of avian visual perception predicts behavioural rejection responses to foreign egg colours

How do birds tell the colours of their own and foreign eggs apart? We demonstrate that perceptual modelling of avian visual discrimination can predict behavioural rejection responses to foreign eggs in the nest of wild birds. We use a photoreceptor noise-limited colour opponent model of visual perception to evaluate its accuracy as a predictor of behavioural rates of experimental egg discrimination in the song thrush Turdus philomelos. The visual modelling of experimental and natural eggshell colours suggests that photon capture from the ultraviolet and short wavelength-sensitive cones elicits egg rejection decisions in song thrushes, while inter-clutch variation of egg coloration provides sufficient contrasts for detecting conspecific parasitism in this species. Biologically realistic sensory models provide an important tool for relating variability of behavioural responses to perceived phenotypic variation.     

鸟类巢寄生伤害理论的进化

鸟类巢寄生的寄主无论是成乌还是雏鸟,对宿主都是极具伤害性的,因为它们降低了宿主的生育力,然而,无论是在寄主种内还是种间,其伤害性的差异变化很大。综述了以往对这种伤害性差异的各种解释,以往的解释在很大程度上集中在伤害性所带来的利益。认为寄主的伤害性行为可以像病原体的伤害性一样进行分类,伤害性在为寄主带来利益的同时,也伴随着代价,所以,由病原体伤害性进化研究衍生而来的平衡假说,适用于解释鸟类巢寄生伤害理论的进化。     

Modelling the maintenance of egg polymorphism in avian brood parasites and their hosts

In avian brood parasitism, egg phenotype plays a key role for both host and parasite reproduction. Several parrotbill species of the genus Paradoxornis are parasitized by the common cuckoo Cuculus canorus, and clear polymorphism in egg phenotype is observed. In this article, we develop a population genetics model in order to identify the key parameters that control the maintenance of egg polymorphism. The model analyses show that egg polymorphism can be maintained either statically as an equilibrium or dynamically with frequency oscillations depending on the sensitivity of the host against unlike eggs and how the parasite targets host nests with specific egg phenotypes. On the basis of the model, we discuss egg polymorphism observed in parrotbills and other host species parasitized by the cuckoo. We suggest the possibility that frequencies of egg phenotypes oscillate and we appeal for monitoring of cuckoo-host interactions over a large spatiotemporal scale.     

Modelling the arms race in avian brood parasitism

In brood parasitism, interactions between a parasite and its host lead to a co-evolutionary process called an arms race, in which evolutionary progress on one side provokes a further response on the other side. The host evolves defensive means to reduce the impact of parasitism, while the parasite evolves means to counter the host's defence. To gain insights into the co-evolutionary process of the arms race, a model is developed and analysed, in which the host's defence and the parasite's counterdefence are assumed to be genetically determined. First, the effect of parasite counterdefence on host defence is analysed. I show that parasite counterdefence can critically affect the establishment of host defence, giving rise to three situations in the equilibrium state: The host shows (1) no defence, (2) an intermediate level of defence or (3) perfect defence. Based on these results, the evolution of parasite counterdefence is considered in connection with host defence. It is suggested that the parasite can evolve counterdefence to a certain degree, but once it has established counterdefence beyond this, the host gives up its defence against parasitism provided the defence entails some cost to perform. Dynamic aspects of selection pressure are crucial for these results. Based on these results, I propose a hypothetical evolutionary sequence in the arms race, along which interactions between the host and parasite proceed.     

Egg color variation,but not egg rejection behavior,changes in a cuckoo host breeding in the absence of brood parasitism

Interactions between parasitic cuckoos and their songbird hosts form a classical reciprocal “arms race,” and are an excellent model for understanding the process of coevolution. Changes in host egg coloration via the evolution of interclutch variation in egg color or intraclutch consistency in egg color are hypothesized counter adaptations that facilitate egg recognition and thus limit brood parasitism. Whether these antiparasitism strategies are maintained when the selective pressure of parasitism is relaxed remains debated. However, introduced species provide unique opportunities for testing the direction and extent of natural selection on phenotypic trait maintenance and variation. Here, we investigated egg rejection behavior and egg color polymorphism in the red‐billed leiothrix (Leiothrix lutea), a common cuckoo (Cuculus canorus) host, in a population introduced to Hawaii 100 years ago (breeding without cuckoos) and a native population in China (breeding with cuckoos). We found that egg rejection ability was equally strong in both the native and the introduced populations, but levels of interclutch variation and intraclutch consistency in egg color in the native population were higher than in the introduced population. This suggests that egg rejection behavior in hosts can be maintained in the absence of brood parasitism and that egg appearance is maintained by natural selection as a counter adaptation to brood parasitism. This study provides rare evidence that host antiparasitism strategies can change under parasite‐relaxed conditions and reduced selection pressure.     

Persistence of egg recognition in the absence of cuckoo brood parasitism: pattern and mechanism

Broad ecological shifts can render previously adaptive traits nonfunctional. It is an open question as to how and how quickly nonfunctional traits decay once the selective pressures that favored them are removed. The village weaverbird (Ploceus cucullatus) avoids brood parasitism by rejecting foreign eggs. African populations have evolved high levels of within-clutch uniformity as well as individual distinctiveness in egg color and spotting, a combination that facilitates identification of foreign eggs. In a companion study, I showed that these adaptations in egg appearance declined following introductions of weavers into habitats devoid of egg-mimicking brood parasites. Here, I use experimental parasitism in two ancestral and two introduced populations to test for changes in egg rejection behavior while controlling for changes in egg appearance. Introduced populations reject foreign eggs less frequently, but the ability of source and introduced populations to reject foreign eggs does not differ after controlling for the evolution of egg color and spotting. Therefore, egg rejection behavior in introduced populations of the village weaver has been compromised by changes in egg appearance, but there has been no significant decline in the birds' ability to recognize foreign eggs. This result reconciles earlier studies on this system and provides insights into the ways behavior can change over generations, especially in the context of recognition systems and the avoidance of brood parasitism.     

Host defense in Nicrophorus quadripunctatus against brood parasitism by Ptomascopus morio (Coleoptera: Silphidae: Nicrophorinae)

Few studies have been conducted on the host defenses of insects against brood parasitism. We investigated whether the silphid beetle Ptomascopus morio, a brood parasite of related silphid species Nicrophorus concolor, can also parasitize another silphid species Nicrophorus quadripunctatus and the manner in which N. quadripunctatus defends itself against parasitism. Successful brood parasitism under natural conditions was not observed at the time of year when P. morio and N. quadripunctatus are both reproductively active. Follow-up experiments revealed that P. morio attempts to oviposit near N. quadripunctatus nests, but is rarely successful if adult hosts are present. When P. morio larvae were experimentally introduced to N. quadripunctatus broods, some P. morio larvae survived when the host and parasite larvae were at the same stage. We concluded that N. quadripunctatus defends itself against brood parasitism in two ways: (1) potential brood parasites are repelled, thus limiting their access to the resource; and (2) the young of the parasitic species are killed.     

On the origin of brood parasitism in altricial birds

The probability that obligate interspecific brood parasitism(OP), among altricial birds evolved directly from the normalbreeding (no parasitism, NP) mode or indirectly through intraspecificnest parasitism (INP) was examined by using maximum-likelihoodand parsimony approaches. We examined the probability of ancestralstates at 24 key nodes in order to test our hypotheses. Thestate of the most basal node in a tree of 565 genera of altricialbirds is equivocal; however, the state probability of NP atthis node is about 5.5-fold more likely than the state of obligateparasite. A similar trend was observed for basal nodes of mostfamilies examined. The INP state was supported only in the Hirundinidae.The high incidence of INP among martins and swallows explainsthis finding. Contrary to our predictions, even in other groupswhere there is a high incidence of INP and OP, such as in thetribe Icteri and the Old World finches, the probability of NPbeing ancestral was very high. We conclude that in all casesbut one (Hirundinidae) obligate, and probably facultative, broodparasitism evolved directly from normal breeding mode ratherthan indirectly through some other form of parasitism.     

The evolution of egg size in the brood parasitic cuckoos

We compared genera of nonparasitic cuckoos and two groups ofparasitic cuckoos: those raised together with host young ("nonejectors")and those in which the newly hatched cuckoo either ejects thehost eggs or chicks, or kills the host young ("ejectors"). Nonejectorsare similar to their hosts in body size and parasitize largerhosts than do ejectors, which parasitize hosts much smallerthan themselves. In both types of parasite, the cuckoo's eggtends to match the host eggs in size. To achieve this, nonejectorshave evolved a smaller egg for their body size than have nonparasiticcuckoos, and ejectors have evolved an even smaller egg. Amongejector cuckoo genera, larger cuckoos have larger eggs relativeto the eggs of their hosts, and the relationship between cuckooegg volume (mass of the newly-hatched cuckoo) and host egg volume(mass to be ejected) did not differ from that predicted by weight-liftingallometry. However, comparing among Cuculus cuckoo species,the allometric slope differed from the predicted, so it is notclear that egg size is related to the need to give the cuckoochick sufficient strength for ejection. Comparing the two mostspeciose ejector genera, Chrysococcyx cuckoos (smaller and parasitizedome-nesting hosts) lay eggs more similar in size to their host'seggs than do Cuculus cuckoos (larger and parasitize open cup–nestinghosts). Closer size-matching of host eggs in Chrysococcyx mayreflect the following: (1) selection to reduce adult body massto facilitate entry through small domed nest holes to lay, and(2) less need for a large egg, because longer incubation periodsin dome-nesting hosts allow the young cuckoo more time to growbefore it need eject host eggs.     

Nest sanitation behavior does not increase the likelihood of parasitic egg rejection in herring gulls

Birds’ behavioral response to brood parasitism can be influenced not only by evolution but also by context and individual experience. This could include nest sanitation, in which birds remove debris from their nests. Ultimately, nest sanitation behavior might be an evolutionary precursor to the rejection of parasitic eggs. Proximately, the context or experience of performing nest sanitation behavior might increase the detection or prime the removal of parasitic eggs, but evidence to date is limited. We tested incubation-stage nests of herring gulls Larus argentatus to ask whether nest sanitation increased parasitic egg rejection. In an initial set of 160 single-object experiments, small, red, blocky objects were usually rejected (18 of 20 nests), whereas life-sized, 3D-printed herring gull eggs were not rejected whether red (0 of 20) or the olive-tan base color of herring gull eggs (0 of 20). Next, we simultaneously presented a red, 3D-printed gull egg and a small, red block. These nests exhibited frequent nest sanitation (small, red block removed at 40 of 48 nests), but egg rejection remained uncommon (5 of those 40) and not significantly different from control nests (5 of 49) which received the parasitic egg but not the priming object. Thus, performance of nest sanitation did not shape individuals’ responses to parasitism. Interestingly, parents were more likely to reject the parasitic egg when they were present as we approached the nest to add the experimental objects. Depending on the underlying mechanism, this could also be a case of experience creating variation in responses to parasitism.     

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.     

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

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

A game theoretical approach to conspecific brood parasitism

We constructed a game theoretical model to predict optimal patternsof egg laying in systems where individuals lay in the nestsof others as well as in their own nests. We show that decreasingthe effect of position within an egg-laying sequence on theworth of an egg should lead to reduced parasitism. Indeed,parasitism can only flourish if the worth of an egg to its biological parent declines with the total number of eggs laid in that nest.Further, we found that increasing the intrinsic costs of eggproduction should lead to an increased propensity for conspecificbrood parasitism. The model also predicts that variation inhosts' ability to reject parasitic eggs has little effect on parasitism until this ability is well developed.     

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

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

Inter‐specific brood parasitism and the evolution of avian reproductive strategies

Avian brood parasitism is a potent selective agent modulating host behaviors and morphology, although its role in determining diversification of avian breeding strategies remains elusive. Hitherto, the study of selection of brood parasites on host breeding strategies has been based on single reproductive trait approaches, which neglect that evolutionary responses to brood parasites may involve co‐ordinated changes in several aspects of reproduction. Here I consider covariation among reproductive traits to test whether parental breeding strategies of hosts of brown headed cowbird (BHC hereafter) in North America and the common cuckoo (CC hereafter) in Europe, two parasites with contrasting level of virulence, have evolved in response to brood parasitism. The effect of parasitism on avian breeding strategies differed between continents. Long term exposure to BHC parasitism selected for a lower breeding investment in North America, but not so CC parasitism in Europe. These results suggest a key role of parasite virulence on the evolution of avian breeding strategies and that brood parasitism has selected for a co‐ordinated breeding strategy of reducing parasitism costs by shortening and fractioning reproductive events within a single season in North America.     

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.     

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.