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.     

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.     

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.     

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.     

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.     

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

Costs and response to conspecific brood parasitism by colonial red-breasted mergansers

Costs of conspecific brood parasitism (CBP) are expected to be influenced by a species’ life history traits. Precocial birds lay large clutches, and clutches that have been enlarged by CBP can affect host fitness through a longer incubation period, displaced eggs, and lower hatching success. We examined costs and response to CBP by hosts in a population of colonial red-breasted mergansers (Mergus serrator; n?=?400 nests over 8 years) within which 29% of parasitized clutches were enlarged considerably (≥?15 eggs). Length of the incubation period did not increase with clutch size. The mean number of eggs displaced from a parasitized nest during incubation (2.8) was 2×?greater than at an unparasitized nest (1.4). Hatching success declined by 2% for each additional egg in the nest. Thus, for a nest with?≥?15 eggs, one or more fewer host eggs hatch relative to an unparasitized nest with the same number of host eggs, assuming equal probability of success for all eggs. Hosts were 40% more likely to desert nests receiving 2 or 6 experimental eggs relative to unparasitized control nests, although it is unknown whether hens deserting a nest renested elsewhere. Our study indicates that costs of CBP to hosts during nesting may be limited to those red-breasted mergansers incubating the largest clutches (≥?15 eggs), and it raises questions about the adaptive significance of deserting a parasitized clutch.     

The evolution of brood parasitism: the role of facultative parasitism

The hypothesis that facultative brood parasitism may serve asan intermediate step in the evolutionary transition from purelyparental reproduction to obligate parasitism was investigated.The population dynamics of a host-parasite complex were computer-simulatedin a model that incorporated different intensities of parasitismand host defense and considered a simplified semelparous birdspecies living in a homogeneous habitat The individuals usetwo different breeding strategies: provide parental care orparasitize the nest of those providing parental care. Underobligate parasitism, the parasites appeared unsuccessful, drovethe host population to extinction, or coexisted with the hostin stable or oscillating proportions. The behavior of the systemdepended on both the effectiveness of the parasite and the defenseof the host. Under facultative parasitism (making the best ofa bad job), the parasites reduced host numbers but did not reducethe population size below the number of breeding sites. Thus,facultative parasitism provides a better opportunity for thedevelopment of defense in the host. The population of a hostthat shows a certain level of defense can be more successfullyinvaded by obligate parasites so that stable coexistence ofhosts and parasites is possible.     

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.     

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。     

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.     

The evolution of obligate interspecific brood parasitism in birds

We present a simple analytical model to investigate the conditionsfor the evolution of obligate interspecific brood parasitismin birds, based on clutch size optimization, when birds canlay more eggs than their optimal clutch size. The results showthat once intraspecific parasitism has appeared (i.e., femalesstart to spread their eggs over their own and other nests) the evolutionarily stable number of eggs laid in its own nest decreases.Two possible ESSs exist: (1) either the evolutionarily stablenumber of eggs laid in its own nest is larger than zero, anda fraction of the total number of eggs is laid parasitically(i.e., intraspecific parasitism); and (2) either the evolutionarilystable number of eggs laid in its own nest is zero and all eggs are laid parasitically. Since all females lay parasitically,this could favor the evolution of obligate interspecific broodparasitism. The key parameter allowing the shift from intraspecificto obligate interspecific parasitism is the intensity of density-dependentmortality within broods (i.e., nestling competition). Strongnestling competition, as in altricial species, can lead toan ESS where all eggs are laid parasitically. Altricial speciesare, therefore, predicted to evolve more easily toward obligate interspecific parasitism than precocial species. These predictionsfit the observed distribution of brood parasitism in birds,where only one species out of 95 obligate interspecific parasitesexhibits a precocial mode of development. Different nestlingsurvival functions provided similar findings (i.e., obligatebrood parasitism is more likely to evolve in altricial species),suggesting that these results are robust with respect to themain assumption of the model.     

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.     

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.     

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.     

Experimental support for the role of nest predation in the evolution of brood parasitism

In 1965, Hamilton and Orians (HO) hypothesized that the starting point for the evolution of obligate interspecific brood parasitism in birds was the facultative laying of physiologically committed eggs in neighbouring active nests of con‐ and heterospecifics, following predation of a bird’s own nest during the laying stage. We tested this prediction of the HO hypothesis by using captive pairs of zebra finches (Taeniopygia guttata), a species with evidence for intraspecific parasitism both in the wild and in captivity. As predicted, in response to experimental nest removal, subjects laid eggs parasitically in simulated active conspecific nests above chance levels. Across subsequent trials, we detected both repeatability and directional change in laying patterns, with some subjects switching from parasitism to depositing eggs in the empty nest. Taken together, these results support the assumptions and predictions of the HO hypothesis, and indicate that the zebra finch is a potential model species for future behavioural and genetic studies in captive brood parasite research.