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.     

Relatedness and the evolution of conspecific brood parasitism

In conspecific brood parasitism (CBP), a parasitic female takes advantage of the parental care performed by a host female by laying eggs in the nest of the host. The host female raises the offspring of the parasitic female as well as her own. In species where local females are related, direct costs for the host might be more than compensated for by gains in inclusive fitness through increased reproduction of a related parasite, but the role of relatedness in CBP is debated. This inclusive-fitness model of parasitism, structured as a game between host and parasite, suggests that both females can gain inclusive fitness and that host-parasite relatedness can therefore facilitate the evolution of CBP. Crucial assumptions are that there is kin discrimination and a potential for host resistance to parasitism by unrelated females but close relatives are accepted. The cost of parasitism in terms of reduced clutch size or offspring survival for the host must not be large; otherwise, parasitism will reduce her inclusive fitness. Therefore, if these costs are high, it does not benefit a host to accept a parasite, even if the parasite is closely related. The secondary female may still have higher fitness from parasitism, but if the costs are high, she should parasitize an unrelated host, not a relative. This requires that the reduction in parasite success that a host can cause by resistance is not too large; otherwise, it will be better for the secondary female to parasitize an accepting related host or to nest solitarily. For these reasons, host-parasite relatedness is most likely to occur in animals where costs of being parasitized are low and host resistance can markedly reduce the success of an unrelated parasite. When costs are higher, parasitism of unrelated hosts may be better, and if host resistance strongly reduces parasite success, solitary breeding is preferable. In some cases, CBP is directly advantageous for the host, and it may sometimes evolve in close connection with cooperative breeding, which is also considered in the model. Some but not all empirical results support these ideas, and more detailed studies of behavior, relatedness, and reproduction of host and parasite are needed for critical tests.     

A framework for modelling and analysing conspecific brood parasitism

Recently several papers that model parasitic egg-laying by birds in the nests of others of their own species have been published. Whilst these papers are concerned with answering different questions, they approach the problem in a similar way and have a lot of common features. In this paper a framework is developed which unifies these models, in the sense that they all become special cases of a more general model. This is useful for two main reasons; firstly in order to aid clarity, in that the assumptions and conclusions of each of the models are easier to compare. Secondly it provides a base for further similar models to start from. The basic assumptions for this framework are outlined and a method for finding the ESSs of such models is introduced. Some mathematical results for the general, and more specific, models are considered and their implications discussed. In addition we explore the biological consequences of the results that we have obtained and suggest possible questions which could be investigated using models within or very closely related to our framework.M. Broom is also a member of the Centre for the Study of Evolution at the University of Sussex.     

The relative role of relatives in conspecific brood parasitism

Conspecific brood parasites lay their eggs in the nests of other females in the same population, leading to a fascinating array of possible ‘games’ among parasites and their hosts ( Davies 2000 ; Lyon & Eadie 2008 ). Almost 30 years ago, Andersson & Eriksson (1982) first suggested that perhaps this form of parasitism was not what it seemed—indeed, perhaps it was not parasitism at all! Andersson & Eriksson (1982) observed that conspecific brood parasitism (CBP) was disproportionally common in waterfowl (Anatidae), a group of birds for which natal philopatry is female‐biased rather than the more usual avian pattern of male‐biased natal philopatry. Accordingly, Andersson (1984) reasoned (and demonstrated in an elegantly simple model) that relatedness among females might facilitate the evolution of CBP—prodding us to reconsider it as a kin‐selected and possibly cooperative breeding system rather than a parasitic interaction. The idea was much cited but rarely tested empirically until recently—a number of new studies, empowered with a battery of molecular techniques, have now put Andersson’s hypothesis to the test ( Table 1 ). The results are tantalizing, but also somewhat conflicting. Several studies, focusing on waterfowl, have found clear evidence that hosts and parasites are often related ( Andersson & Åhlund 2000 ; Roy Nielsen et al. 2006 ; Andersson & Waldeck 2007 ; Waldeck et al. 2008 ; Jaatinen et al. 2009 ; Tiedemann et al. 2011 ). However, this is not always the case ( Semel & Sherman 2001 ; Anderholm et al. 2009 ; and see Pöysa 2004 ). In a new study reported in this issue of Molecular Ecology, Jaatinen et al. (2011a) provide yet another twist to this story that might explain not only why such variable results have been obtained, but also suggests that the games between parasites and their hosts—and the role of kinship in these games—may be even more complex than Andersson (1984) imagined. Indeed, the role of kinship in CBP may be very much one of relative degree!

Table 1. A summary of recent studies that have tested for evidence of relatedness between hosts and parasites in avian conspecific brood parasites

Responses of Black-headed Gulls Larus ridibundus to conspecific brood parasitism

Conspecific brood parasitism in birds occurs when a female inserts her egg into the clutch of her own species. If successful, i.e. the parasitic egg is accepted by the host, then the host female or pair rears the offspring of the parasite. In the present study, we studied natural conspecific brood parasitism in Black-headed Gulls (Larus ridibundus), and conducted series of the experiments with mimetic (conspecific) and non-mimetic (conspecific painted light blue) eggs to explore responses of the tested pairs towards these alien eggs. The natural parasitism rate was 10% and the probability of being parasitized significantly increased with nest density. Experimentally parasitized pairs rejected both types of experimental eggs at a similar rate: 14.3 % for mimetic and 25.5% for non-mimetic within 2 days. Non-mimetic eggs were more selectively rejected than mimetic eggs. The relationships between the probability of egg rejection (dependent variable) and predictor (independent) variables were examined by fitting generalized linear models. Contrast and intraclutch variation in ground color and spotting pattern and the volume of the egg had no significant effect on rejection behavior in either non-mimetic or mimetic eggs. However, nest density significantly positively affected rejection behavior of the Black-headed Gulls in both non-mimetic and mimetic treatments.     

The role of kin recognition in the evolution of conspecific brood parasitism

Conspecific brood parasitism (CBP) is a common strategy in several species of birds. Currently, some studies suggest that relatedness between host and parasite enhances CBP, since indirect fitness benefits could select for acceptance of related eggs by hosts. Conversely, parasites should avoid laying eggs in nests of relatives if this is costly for the host. Based on the latter argument, kinship should not promote brood parasitism. A recent model clarified this relationship, and showed that kinship can promote brood parasitism, assuming kin recognition. However, in that model kin recognition was assumed perfect. Here we present a model that addresses the role of relatedness and kin selection in CBP, when kin recognition is not perfect and hosts do not always detect parasitism. We consider both the indirect fitness of the parasite and the possible responses of the host. Our results indicate that the existence and accuracy of a kin recognition system is crucial to the final outcome. When CBP represents a cost to the host, a parasitic female that has the choice should avoid parasitizing relatives, unless (1) the costs are not too high and (2) hosts can accurately enough recognize eggs laid by relatives, rejecting them less often than eggs laid by nonkin. But if ‘parasitism’ enhances the direct fitness of the host (which is possible in species with precocial young) parasites should choose relatives whenever possible, even if hosts do not recognize kin eggs. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Nest predation and the evolution of conspecific brood parasitism: from risk spreading to risk assessment

Conspecific brood parasitism (CBP) is a taxonomically widespread reproductive tactic. One of the earliest hypotheses put forward to explain the evolution of CBP was "risk spreading"; that is, by laying eggs in more than one nest, parasites may increase the likelihood that at least one offspring will survive to independence. However, the risk spreading hypothesis, based on the assumptions of random nest predation and random selection of target nests by parasites, was theoretically refuted soon after its appearance. New results from the common goldeneye (Bucephala clangula) have revealed that nests are not predated at random and that parasites preferentially lay in safe nests. By taking into account these findings and by modifying accordingly the basic assumptions of the earlier model that refuted the risk spreading hypothesis, we built a model to address the role of nest predation in the evolution of CBP. Model simulations revealed that the selective advantage of parasitic laying, related to nest predation, is much higher than previously thought. Furthermore, the invasion probability of parasitic tactic when initially rare was reasonably high within our model framework. We show that the use of risk assessing, instead of random risk spreading, makes parasitic laying evolutionarily advantageous.     

Detecting conspecific brood parasitism using egg morphology in black brant Branta bernicla nigricans

Numerous methods have been proposed to indirectly detect conspecific brood parasitism (CBP) in birds. Egg morphology has been suggested as a predictor of parasitism, assuming that variation in egg size is greater among females than within females. Here we use microsatellite data to assess the use of egg morphology to detect CBP in a sample of black brant Branta bernicla nigricans nests. We attempted to repeat a previously demonstrated technique using cluster analysis and maximum Euclidean distance (MED) to detect parasitized nests within black brant. Additionally we attempted a new technique based on a discriminant function analysis of egg morphology in an attempt to detect brood parasitic eggs. When detecting parasitized nests using egg morphology, the cluster analysis revealed that the MED between the two most dissimilar eggs in each nest was significantly greater for parasitized nests than for non‐parasitized nests (1.62±0.06 and 1.43±0.08, respectively). The extent of overlap in sizes of eggs between parasitized and non‐parasitized nests, however, was such that we were unable to effectively identify parasitized nests. In most cases for each parasitized nest correctly identified, 3 non‐parasitized nests were incorrectly identified as parasitic. When we attempted to detect parasitic eggs we found that parasitic eggs were more different from the expected egg volume than host eggs: mean absolute residual volume of parasitic eggs=2.59±5.79 cm³ while that for host eggs=1.82±2.14 cm³. Overall, we found that the discriminant function analysis was moderately effective in determining whether eggs belonged to the host female using a resubstitution technique (error rate=9.71%) or a jackknife technique (error rate=6.12%). Additionally, we found a higher but moderate error rate when using an independent data set to validate the function (error rate=14.07%). In both cases, however, parasitic eggs accounted for most of the error and were not correctly classified 75%, 70% and 100% of the time respectively. We suggest when developing a predictive function for detecting conspecific brood parasitism based on egg morphology that an appropriate technique be used to validate the function, particularly those techniques that utilize unambiguous identifiers such as molecular and protein fingerprinting techniques.     

Reliability of egg morphology to detect conspecific brood parasitism in goldeneyes Bucephala clangula examined using protein fingerprinting

Eadie (1989) developed a method based on variation between females in egg length, width and weight to detect conspecific brood parasitism in the field: using these three egg measures, Euclidean distance between all pairs of eggs within a clutch is calculated, and if maximum Euclidean distance (MED) between any two eggs exceeds a threshold value the nest is considered parasitized. The MED method has been tested in Finnish and Scottish common goldeneye Bucephala clangula populations but the results have been contradicting. Here we use protein fingerprinting to assess the validity of the MED method. Data comprised 35 clutches of which we knew, based on protein fingerprinting, how many different females laid the clutch (range 1–5 females). The mean MED of non-parasitized clutches (laid by 1 female only) was 1.470 (95% CI: lower 1.169, upper 1.771; n=21) and that of parasitized clutches (laid by 2 or more females) was 3.654 (95% CL: lower 3.083, upper 4.225; n=14). Using a MED>3.0 as a criterion to identify parasitized clutches 89% of all clutches were classified correctly either parasitized or non-parasitized when compared to the identification based on protein fingerprinting. Clutch size and the number of females (beyond 2 females) did not affect the clutch MED, whereas the status of parasitism did. Repeatability of egg length, width and weight were: 0.63, 0.76 and 0.80, respectively, implying that, variation in these egg measures occurs among rather than within females. Our new results confirm that the MED method is reliable enough to detect parasitism in common goldeneye.     

Carlin tag recoveries as an indicator of predation on salmon smolts by goosanders and red-breasted mergansers

Between 1984 and 1990 a total 221 Carlin tags used to mark salmon Salmo salar smolts in the River North Esk, NE Scotland, were recovered from the stomachs of goosanders Mergus merganser and red-breasted mergansers M. serrator . Both Carlin-tagging and adipose-clipping affected the predation of salmon smolts by sawbill ducks. The mean (± S.D.) sizes of tagged smolts taken by both species were similar (117 ± 3 mm) and significantly smaller than the mean sizes of smolts in the river, possibly due to a reduction in the swimming performance of small smolts bearing tags. Large adipose-clipped smolts (±mean smolt size) were predated significantly more than unclipped smolts, but no such difference was observed for small smolts (相似文献   

Kin grouping is insufficient to explain the inclusive fitness gains of conspecific brood parasitism in the common eider

Conspecific brood parasitism allows females to exploit other females' nests and enhance their reproductive output. Here, we test a recent theoretical model of how host females gain inclusive fitness from brood parasitism. High levels of relatedness between host and parasitizer can be maintained either by: (a) kin recognizing and parasitizing each other as a form of cooperative breeding or (b) natal philopatry and nest site fidelity facilitating the formation of kin groups, thereby increasing the probability of parasitism between relatives nesting in close proximity. To address these two hypotheses we genotyped feathers and hatch membranes of common eiders (Somateria mollissima) from western Hudson Bay, Canada, using a noninvasive sampling methodology. We found that most instances of brood parasitism do result in inclusive fitness gains. Furthermore, females with failed nests moved an average of 492 m from their previous year's nest site, while successful females only moved an average of 13 m. Therefore, we observed host–parasite relatedness can occur at levels higher than would be expected by chance even in the absence of kin grouping, suggesting that closely related females nesting near one another is not essential to maintain high host–parasitizer relatedness. In addition, kin grouping is only a transient phenomenon that cannot occur every year due to the propensity for females of failed nests to nest farther away from their nest site in subsequent years than females with successful nests, which provides support for kin recognition as a more likely mechanism to maintain high host–parasitizer relatedness over time.     

Indirect evidence of conspecific nest parasitism in the colonial whiskered tern (Chlidonias hybrida)

Conspecific nest parasitism (CNP) is widespread among birds and is particularly common in colonial species. Nevertheless, this reproductive tactic is remarkably little described in terns. In this study we use egg morphology as indirect evidence of CNP in the whiskered tern (Chlidonias hybrida) in 17 colonies from two French populations. We study CNP with respect to the duration of egg laying (i.e. clutch size), and also present some behavioural aspects that could facilitate CNP. From the inspection of 121 two-egg, 279 three-egg and 11 more egg-clutches, we detected a minimum %CNP of 9.2% for the two study populations, combined with large differences between the two populations (4.0% vs. 14.5% in three-egg clutches) and between colonies (0 up to 30%). %CNP was significantly higher in three-egg (9.0%) than in two-egg clutches (1.7%), suggesting that duration of egg laying is a determining factor of parasitism. The rather high %CNP detected in this species might be facilitated by (1) the observed long unattendance of nest by any of the pair members, mainly during the pre-incubation period, and (2) high synchrony in laying dates within colonies. A possible link between nest density and CNP rate was suggested. Finally, we encourage new investigations of CNP in other tern species.     

No evidence for a negative effect of conspecific brood parasitism on annual survival of female Prothonotary Warblers

Species that provide intensive parental care could suffer fitness costs associated with conspecific brood parasitism. Here we evaluate the effect of conspecific brood parasitism on apparent annual survival probability of female Prothonotary Warblers Protonotaria citrea using a multistate model with imperfect state assignment analysed in a hierarchical Bayesian framework. We found no difference in annual survival probability between host and non‐host females. These findings agree with previous work in that there seems to be little apparent cost of conspecific brood parasitism to female Warblers in this system.     

Evolution of tolerance by magpies to brood parasitism by great spotted cuckoos

Hosts may use two different strategies to ameliorate negative effects of a given parasite burden: resistance or tolerance. Although both resistance and tolerance of parasitism should evolve as a consequence of selection pressures owing to parasitism, the study of evolutionary patterns of tolerance has traditionally been neglected by animal biologists. Here, we explore geographical covariation between tolerance of magpies (Pica pica) and brood parasitism by the great spotted cuckoo (Clamator glandarius) in nine different sympatric populations. We estimated tolerance as the slope of the regression of number of magpie fledglings (i.e. host fitness) on number of cuckoo eggs laid in non-depredated nests (which broadly equals parasite burden). We also estimated prevalence of parasitism and level of host resistance (i.e. rejection rates of mimetic model eggs) in these nine populations. In accordance with the hypothetical role of tolerance in the coevolutionary process between magpies and cuckoos we found geographical variation in tolerance estimates that positively covaried with prevalence of parasitism. Levels of resistance and tolerance were not associated, possibly suggesting the lack of a trade-off between the two kinds of defences against great spotted cuckoo parasitism for magpies. We discuss the results in the framework of a mosaic of coevolutionary interactions along the geographical distribution of magpies and great spotted cuckoos for which we found evidence that tolerance plays a major role.     

Relatedness and the evolution of conspecific brood parasitism: parameterizing a model with data for a precocial species

Conspecific brood parasitism (CBP) is a common reproductive tactic in several animal taxa, especially in precocial birds. It has been suggested that host-parasite relatedness can facilitate the evolution of CBP. A recent model showed that the existence and accuracy of the kin recognition system is crucial for this to occur. I used field data to parameterize the model for the common goldeneye, Bucephala clangula, a precocial species in which CBP frequently occurs and in which a recent finding of nonrandom host-parasite relatedness has been interpreted to support the idea that relatedness and kin selection influence CBP. It turned out that possibilities to detect brood parasitism and accurately discriminate between kin and nonkin parasites are negligible in the species. The empirically parameterized model exercise revealed that relatedness and kin selection are unlikely explanations of CBP in the species.