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.     

Brood parasitism,female condition and clutch reduction in the common eider Somateria mollisima

Conspecific brood parasitism (CBP) is an alternative reproductive tactic found in many animals with parental care. Parasitizing females lay eggs in the nests of other females (hosts) of the same species, which incubate and raise both their own and the foreign offspring. The causes and consequences of CBP are debated. Using albumen fingerprinting of eggs for accurately detecting parasitism, we here analyse its relation to female condition and clutch size in High Arctic common eiders Somateria mollissima borealis. Among 166 clutches in a Svalbard colony, 31 (19%) contained eggs from more than one female, and 40 of 670 eggs (6%) were parasitic. In 6 cases an active nest with egg(s) was taken over by another female. Many suitable nest sites were unoccupied, indicating that CBP and nest takeover are reproductive tactics, not only consequences of nest site shortage. Similarity in body mass between female categories suggests that condition does not determine whether a nesting female becomes parasitised. There was no evidence of low condition in parasites: egg size was similar in hosts and parasites, and parasitism was equally frequent early and late in the laying season. Meta‐analysis of this and 3 other eider studies shows that there is a cost of being parasitised in this precocial species: host females laid on average 7% fewer eggs than other females.     

Conspecific brood parasitism and egg quality in blue tits Cyanistes caeruleus

Laying eggs in nests of unrelated conspecific pairs to parasitize their parental care is a common phenomenon in birds. In blue tits Cyanistes caeruleus such conspecific brood parasitism (CBP) has never been reported in the literature. However, in a situation where breeding density was extremely high, we found six nests to be parasitized with eggs of conspecific females. Natural selection may favour elevated competitiveness of parasite young, since the negative consequences of increased sibling competition are incurred on the unrelated host parents and siblings, and therefore do not act as inclusive fitness costs for the parasites. Parasitizing females could achieve such a competitive advantage for their offspring by laying larger eggs or eggs with higher concentrations of testosterone in the yolk. We analyzed these parameters of the six parasitized nests, but did not find that parasite eggs differ systematically in these aspects from host eggs, nor that parasite eggs showed resemblance to host eggs. We suggest that a shortage of available nest sites caused some females to use CBP as a best-of-a bad job strategy, but that either the occurrence of CBP is too rare to lead to strong selection for egg adjustments or that parasitizing females are unable to do so.     

Colony kin structure and host‐parasite relatedness in the barnacle goose

Conspecific brood parasitism (CBP), females laying eggs in the nest of other ‘host’ females of the same species, is a common alternative reproductive tactic among birds. For hosts there are likely costs of incubating and rearing foreign offspring, but costs may be low in species with precocial chicks such as waterfowl, among which CBP is common. Waterfowl show strong female natal philopatry, and spatial relatedness among females may influence the evolution of CBP. Here we investigate fine‐scale kin structure in a Baltic colony of barnacle geese, Branta leucopsis, estimating female spatial relatedness using protein fingerprints of egg albumen, and testing the performance of this estimator in known mother‐daughter pairs. Relatedness was significantly higher between neighbour females (nesting ≤ 40 metres from each other) than between females nesting farther apart, but there was no further distance trend in relatedness. This pattern may be explained by earlier observations of females nesting close to their mother or brood sisters, even when far from the birth nest. Hosts and parasites were on average not more closely related than neighbour females. In 25 of 35 sampled parasitized nests, parasitic eggs were laid after the host female finished laying, too late to develop and hatch. Timely parasites, laying eggs in the host’s laying sequence, had similar relatedness to hosts as that between neighbours. Females laying late parasitic eggs tended to be less related to the host, but not significantly so. Our results suggest that CBP in barnacle geese might represent different tactical life‐history responses.     

Brood parasitic European starlings do not lay high-quality eggs

Chicks of obligate brood parasites employ a variety of morphologicaland behavioral strategies to outcompete nest mates. Elevatedcompetitiveness is favored by natural selection because parasiticchicks are not related to their host parents or nest mates.When chicks of conspecific brood parasites (CBPs) are unrelatedto their hosts, they and their parents would also benefit fromtraits that enhance competitiveness. However, these traits mustbe inducible tactics in CBPs, since conspecific brood parasitism(CBP) is facultative. Such tactics could be induced by resourcespassed to offspring through the egg. Thus, females engagingin CBP should allocate to their eggs resources that will enhanceoffspring competitiveness. We tested this prediction in a populationof European starlings (Sturnus vulgaris) breeding in southernSweden. Previous research showed that almost all CBPs in thispopulation are floater females that have yet to breed in thecurrent season. We identified putative brood parasitic eggsthrough monitoring egg laying and verified parasitism usingprotein fingerprinting. We then determined whether parasiticeggs were larger, larger-yolked, or had higher concentrationsof yolk testosterone or androstenedione than control eggs. The14 brood parasitic eggs laid in active nests (those with clutchesof at least two eggs that were eventually incubated) did notdiffer from controls in any of these characteristics. Ten dumpedeggs, laid in nonactive nest-boxes or on the ground, were smallerand smaller-yolked than control eggs but did not differ in yolkandrogen concentrations. The failure of our prediction couldbe the result of high costs of investing in eggs, lack of competition-basedbenefits for chicks, or physiological constraints on egg manipulation.     

Relative reproductive success of female moorhens using conditional strategies of brood parasitism and parental care

In a population of moorhens (Gallinula chloropus), at least27% of netting females laid one or more eggs in a neighbor'snest Females laid parasitically under three conditions: 56%of parasitic eggs were from nesting females that preceded layinga dutch in their own nest by a parasitic laying bout, 19% werefrom females whose nests were depredated before clutch completionand that laid the following egg parasiticaDy, and 25% were froma small number of females without territories, "non-nesting"parasites, that each laid a series of parasitic eggs. Clutchsizes varied greatly between females, but nesting females eachlaid a consistent clutch size both within and between seasonsfor a given mate and territory. Nesting females that employeda dual strategy of brood parasitism and parental care producedextra eggs that they laid in the nests of neighbors before layinga dutch in their own nests. Two out of ten females whose dutchesI experimentally removed during the laying period were successfullyinduced to lay their next egg in the nest of a neighbor. Nestingfemales that laid parasitically selected their hosts opportunisticallyfrom among the nests dosest to their territories. An experimentin which parasitic eggs were removed and hosts left to rearonly their own young showed that parasites did not choose hoststhat were better parents than pairs with contemporary neststhat were not parasitized. Females that only laid parasiticaDywithin a given season timed their parasitic laying bouts poorlyand achieved no reproductive success. Parasitic young rarelyfledged, and the mean seasonal reproductive success of nestingbrood parasites did not differ from that of nonparasitic females.However, the variance in reproductive success of nesting broodparasites was significantly higher than that of nonparasiticfemales.     

Host-parasite kinship in a female-philopatric bird population: evidence from relatedness trend analysis

Conspecific brood parasitism (CBP), an alternative reproductive tactic where some females lay eggs in the nests of other females of the same species, occurs in many animals with egg care. It is particularly common in waterfowl, for reasons that are debated. Many waterfowl females nest near their birthplace, making it likely that some local females are relatives. We analyse brood parasitism in a Hudson Bay population of common eiders, testing predictions from two alternative hypotheses on the role of relatedness in CBP. Some models predict host-parasite relatedness, others predict that parasites avoid close relatives as hosts. To distinguish between the alternatives, we use a novel approach, where the relatedness of host-parasite pairs is tested against the spatial population trend in pairwise relatedness. We estimate parasitism, nest take-over and relatedness with protein fingerprinting and bandsharing analysis of egg albumen, nondestructively sampled from each new egg in the nest throughout the laying period. The results refute the hypothesis that parasites avoid laying eggs in the nests of related hosts, and corroborate the alternative of host-parasite relatedness. With an estimated r of 0.12-0.14, females laying eggs in the same nest are on average closer kin than nesting neighbour females. Absence of a population trend in female pairwise relatedness vs. distance implies that host-parasite relatedness is not only an effect of strong natal philopatry: some additional form of kin bias is also involved.     

Great Spotted Cuckoos Frequently Lay Their Eggs While Their Magpie Host is Incubating

Species that suffer from brood parasitism face a considerable reduction in their fitness which selects for the evolution of host defences. To prevent parasitism, hosts can mob or attack brood parasites when they approach the host nest and block the access to the nest by sitting on the clutch. In turn, as a counter‐adaptation, brood parasites evolved secretive behaviours near their host nests. Here, we have studied great spotted cuckoo (Clamator glandarius) egg‐laying behaviour and defence by their magpie (Pica pica) hosts inside the nest using continuous video recordings. We have found several surprising results that contradict some general assumptions. The most important is that most (71%) of the parasitic events by cuckoo females are completed while the magpie females are incubating. By staying in the nest, magpies force cuckoo females to lay their egg facing the high risk of being attacked by the incubating magpie (attack occurred in all but one of the events, n = 15). During these attacks, magpies pecked the cuckoo violently, but could never effectively avoid parasitism. These novel observations expand the sequence of adaptations and counter‐adaptations in the arms race between brood parasites and their hosts during the pre‐laying and laying periods.     

Common Cuckoos Cuculus canorus change their nest‐searching strategy according to the number of available host nests

In recent decades, numerous studies have examined factors affecting risk of host nest parasitism in well‐known avian host–parasite systems; however, little attention has been paid to the role of host nest availability. In accordance with other studies, we found that nest visibility, reed density and timing of breeding predicted brood parasitism of Great Reed Warblers Acrocephalus arundinaceus by the Common Cuckoo Cuculus canorus. More interestingly, hosts had a greater chance of escaping brood parasitism if nesting was synchronized. Cuckoo nest searching was governed primarily by nest visibility at high host‐nest density. However, even well‐concealed nests were likely to be parasitized during periods when just a few hosts were laying eggs, suggesting that Cuckoos adjust their nest‐searching strategy in relation to the availability of host nests. Our results demonstrate that host vulnerability to brood parasitism varies temporally and that Cuckoo females are able to optimize their nest‐searching strategy. Moreover, our study indicated that Cuckoos always manage to find at least some nests to parasitize. Thus, in this case, the co‐evolutionary arms race should take place mainly in the form of parasitic egg rejection rather than via frontline pre‐parasitism defence.     

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.     

Brood parasitism,relatedness and sociality: a kinship role in female reproductive tactics

Conspecific brood parasitism (CBP) is a reproductive tactic in which parasitic females lay eggs in nests of other females of the same species that then raise the joint brood. Parasites benefit by increased reproduction, without costs of parental care for the parasitic eggs. CBP occurs in many egg‐laying animals, among birds most often in species with large clutches and self‐feeding young: two major factors facilitating successful parasitism. CBP is particularly common in waterfowl (Anatidae), a group with female‐biased natal philopatry and locally related females. Theory suggests that relatedness between host and parasite can lead to inclusive fitness benefits for both, but if host costs are high, parasites should instead target unrelated females. Pairwise relatedness (r) in host–parasite (h‐p) pairs of females has been estimated using molecular genetic methods in seven waterfowl (10 studies). In many h‐p pairs, the two females were unrelated (with low r, near the local population mean). However, close relatives (r = 0.5) were over‐represented in h‐p pairs, which in all 10 studies had higher mean relatedness than other females. In one species where this was studied, h‐p relatedness was higher than between nesting close neighbours, and hosts parasitized by non‐relatives aggressively rejected other females. In another species, birth nest‐mates (mother–daughters, sisters) associated in the breeding area as adults, and became h‐p pairs more often than expected by chance. These and other results point to recognition of birth nest‐mates and perhaps other close relatives. For small to medium host clutch sizes, addition of a few parasitic eggs need not reduce host offspring success. Estimates in two species suggest that hosts can then gain inclusive fitness if parasitized by relatives. Other evidence of female cooperation is incubation by old eider Somateria mollissima females of clutches laid by their relatives, and merging and joint care of broods of young. Merging females tended to be more closely related. Eiders associate with kin in many situations, and in some geese and swans, related females may associate over many years. Recent genetic evidence shows that also New World quails (Odontophoridae) have female‐biased natal philopatry, CBP and brood merging, inviting further study and comparison with waterfowl. Kin‐related parasitism also occurs in some insects, with revealing parallels and differences compared to birds. In hemipteran bugs, receiving extra eggs is beneficial for hosts by diluting offspring predation. In eggplant lace bugs Gargaphia solani, host and parasite are closely related, and kin selection favours egg donation to related females. Further studies of kinship in CBP, brood merging and other contexts can test if some of these species are socially more advanced than presently known.     

Rapid laying by Brown-headed Cowbirds Molothrus ater and other parasitic birds

We compared the length of time parasitic and nonparasitic female birds spent on nests while laying eggs (laying bouts) to evaluate the hypothesis that rapid laving by parasitic Brown-headed Cowbirds Molothrus ater and other parasitic birds is a specialization for brood parasitism. Brown-headed Cowbirds typically spent less than 1 min on host nests while laying (41.0 ± 4.58 [mean ± s.e.] s, n = 21). In contrast, mean laving bouts of six nonparasitic icterine species ranged from 21.5 min to 53.4 min, and laying bouts of 13 other passerine species ranged from 20.7 min to 103.7 min. By spending only a few seconds on the nest while laying, brood parasites probably increase their chances of parasitizing nests unnoticed by hosts or, if noticed, are harassed by hosts for less time. Rapid laying may be adaptive if aggression by hosts can thwart attempted parasitism by chasing away the parasite, preventing the parasite from entering the nest or injuring the parasite. Rapid laying may increase the likelihood that the parasitic egg will be accepted. We tested some of these hypotheses by recording the responses of three frequently parasitized species to a stuffed female cowbird placed on their nests for 1 min. All species attacked the model vigorously; however, the mean time for discovery of the model ranged from 3 min to 17 min, ample time for female cowbirds to parasitize the nests. We concluded that rapid laying by parasitic birds is an adaptation for parasitism and, in Brown-headed Cowbirds, reduces the chances that the parasite will be attacked by hosts.     

Molecular identification of brood‐parasitic females reveals an opportunistic reproductive tactic in ruddy ducks

In many taxa, females lay eggs in the nests of other conspecifics. To determine the conditions under which conspecific brood parasitism develops, it is necessary to identify parasitic offspring and the females who produce them; however, for most systems parasitism can be difficult to observe and most genetic approaches have relatively low resolving power. In this study, we used protein fingerprinting from egg albumen and 10 microsatellite loci to genetically match parasitic ducklings to their mothers in a population of ruddy ducks (Oxyura jamaicensis). We found that 67% of nests contained parasitic offspring, and we successfully identified their mothers in 61% of the cases. Of the parasitic females identified, 77% also had nests of their own (i.e. a dual tactic, where females both nest and lay parasitically), and we found no evidence that parasitic females pursued a specialist (parasitism only) tactic. We also found that parasitic egg laying was not influenced by nest loss, predation or female condition. Thus, in contrast to most waterfowl studied to date, female ruddy ducks appear to lay parasitic eggs whenever the opportunity arises.     

Do parasitic common goldeneye Bucephala clangula females choose nests on the basis of host traits or nest site traits?

Conspecific brood parasitism (CBP) is an important alternative breeding strategy for gaining reproductive output in birds. While interactions between hosts and parasites and consequences of CBP to breeding success of both parties have been studied a lot, the roles of host characteristics and nest site characteristics in CBP have received less attention. We studied the relative importance of host‐related traits, such as female condition and breeding experience, and nest‐site‐related factors, such as overall nest site preference and occupation rate, in explaining the occurrence of CBP in a common goldeneye Bucephala clangula population. We used spatially and temporally extensive data sets, analysed the data with generalized linear mixed models that allowed us to account for the non‐independency of individual nesting attempts across females and nesting sites, and used an information theoretic approach in model selection and inference. About half of the nests were parasitized annually during the seven year study period. The occurrence of CBP decreased with advancement of the breeding season but late nests were also frequently parasitized. We found that the occurrence of CBP was better explained by nest‐site characteristics than host traits, implying that parasitic females target a given nest based on factors related to the nest site itself rather than on the host. Our results suggest that more attention should be paid to factors associated with nest site attractiveness and quality when studying laying decisions of parasites and the occurrence of CBP in general.     

Host switching in cowbird brood parasites: how often does it occur?

Avian obligate brood parasites lay their eggs in nests of host species, which provide all parental care. Brood parasites may be host specialists, if they use one or a few host species, or host generalists, if they parasitize many hosts. Within the latter, strains of host‐specific females might coexist. Although females preferentially parasitize one host, they may occasionally successfully parasitize the nest of another species. These host switching events allow the colonization of new hosts and the expansion of brood parasites into new areas. In this study, we analyse host switching in two parasitic cowbirds, the specialist screaming cowbird (Molothrus rufoaxillaris) and the generalist shiny cowbird (M. bonariensis), and compare the frequency of host switches between these species with different parasitism strategies. Contrary to expected, host switches did not occur more frequently in the generalist than in the specialist brood parasite. We also found that migration between hosts was asymmetrical in most cases and host switches towards one host were more recurrent than backwards, thus differing among hosts within the same species. This might depend on a combination of factors including the rate at which females lay eggs in nests of alternative hosts, fledging success of the chicks in this new host and their subsequent success in parasitizing it.     

Conspecific brood parasitism in the tropics: an experimental investigation of host responses in common moorhens and American purple gallinules

Species occupying a broad latitudinal range may show greater phenotypic plasticity in behavior than species with smaller ranges or more specific habitat requirements. This study investigates for the first time the occurrence of conspecific brood parasitism (CBP) in sympatric tropical populations of the common moorhen (Gallinula chloropus pauxilla Bangs) and the American purple gallinule (Porphyrula martinica L.). CBP occurred in at least 20% (N = 76) of common moorhen nests on the Rio Chagres in Panama. Half (N = 20) of the parasitic eggs were accepted, but 10 were destroyed or ejected from host nests. Introductions of experimental eggs into nests revealed hosts were more likely to accept parasitism later in the host's laying period and during incubation, consistent with expectation of an adaptive response. CBP was not detected in a small sympatric population of American purple gallinules. Members of this population did not eject experimental eggs, suggesting a lack of experience with costly CBP. Contrasting ecological factors help explain why these two species of rail (Family Rallidae) differ in regard to CBP. Purple gallinule territories were sparse, owing to the distribution of preferred habitat. Moorhens flocked outside of the breeding season. They nested more synchronously, at higher densities, and primarily in ephemeral floating vegetation. Further, moorhens suffered a rate of nest loss nearly double that of American purple gallinules, and this increased over the course of the breeding season. Moorhen clutches were larger on average, and more variable in size than those of purple gallinules. Reproductive effort and rate (seasonality) constitute important life history differences between these species that may constrain the evolution of reproductive tactics. Comparing these sympatric populations, and others differing in life-history traits and ecological constraints, highlights the role of risk management in the evolution of CBP.     

Egg morphology fails to identify nests parasitized by conspecifics in common pochard: a test based on protein fingerprinting and including female relatedness

Conspecific brood parasites lay eggs in nests of other females of the same species. A variety of methods have been developed and used to detect conspecific brood parasitism (CBP). Traditional methods may be inaccurate in detecting CBP and in revealing its true frequency. On the other hand more accurate molecular methods are expensive and time consuming. Eadie developed a method for revealing CBP based on differences in egg morphology. That method is based on Euclidean distances calculated for pairs of eggs within a clutch using standardized egg measurements (length, width and weight). We tested the applicability of this method in the common pochard Aythya ferina using nests that were identified as parasitized (39 nests) or non‐parasitized (16 nests) based on protein fingerprinting of eggs. We also analyzed whether we can distinguish between parasitic and host eggs in the nest. We found that variation in MED can be explained by parasitism but there was a huge overlap in MED between parasitized and non‐parasitized nests. MED also increased with clutch size. Using discriminant function analysis (DFA) we found that only 76.4% of nests were correctly assigned as parasitized or non‐parasitized and only 68.3% of eggs as parasitic or host eggs. Moreover we found that MED in parasitized nests increased with relatedness of the females that laid eggs in the nest. This finding was supported by positive correlation between MED and estimated relatedness in female–female pairs. Although variation in egg morphology is associated with CBP, it does not provide a reliable clue for distinguishing parasitized nests from non‐parasitized nests in common pochard.     

The evolution of sexual dimorphism in parasitic cuckoos: sexual selection or coevolution?

Sexual dimorphism is ubiquitous in animals and can result from selection pressure on one or both sexes. Sexual selection has become the predominant explanation for the evolution of sexual dimorphism, with strong selection on size-related mating success in males being the most common situation. The cuckoos (family Cuculidae) provide an exceptional case in which both sexes of many species are freed from the burden of parental care but where coevolution between parasitic cuckoos and their hosts also results in intense selection. Here, we show that size and plumage differences between the sexes in parasitic cuckoos are more likely the result of coevolution than sexual selection. While both sexes changed in size as brood parasitism evolved, we find no evidence for selection on males to become larger. Rather, our analysis indicates stronger selection on parasitic females to become smaller, resulting in a shift from dimorphism with larger females in cuckoos with parental care to dimorphism with larger males in parasitic species. In addition, the evolution of brood parasitism was associated with more cryptic plumage in both sexes, but especially in females, a result that contrasts with the strong plumage dimorphism seen in some other parasitic birds. Examination of the three independent origins of brood parasitism suggests that different parasitic cuckoo lineages followed divergent evolutionary pathways to successful brood parasitism. These results argue for the powerful role of parasite-host coevolution in shaping cuckoo life histories in general and sexual dimorphism in particular.     

Laying eggs in others' nests: Intraspecific brood parasitism in birds

Intraspecific brood parasitism occurs commonly in a large number of bird species. Recent work shows that females parasitize the parental care of conspecifics either as a 'best-of-a-bad-job' strategy or as part of a superior reproductive strategy. A number of parasite and host behaviours, which either facilitate or prevent intraspecific brood parasitism, are similar to those occurring among interspecific brood parasites and their hosts.