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.     

How many eggs should be laid in one's own nest and others’ in intra-specific brood parasitism?

Recent field studies have demonstrated that many bird species practice intra-specific brood parasitism. They lay eggs in the nests of other individuals of the same species, let the foster parents rear their offspring and avoid the cost of parental care. It has been shown that many birds, including starlings, swallows and geese, practice intra-specific brood parasitism in various forms. Intra-specific brood parasitism can be viewed in terms of optimal resource allocation: how many eggs should be put in the nests of other individuals under the risk of being parasitized by others. The situation here is a game, because the fitness of a parasitic individual depends on how other individuals behave (how many individuals practice parasitism and to what extent). The ecology of intra-specific brood parasitism has been investigated extensively by field ornithologists recently and it is full of material for modeling population/evolutionary biology. In this paper, I present a simple individual-based model to challenge the resource allocation problem in intra-specific brood parasitism. Previous theoretical studies of intra-specific brood parasitism have been based on ESS or quantitative genetics models, where a population is implicitly assumed to be homogeneous and the distribution form of the trait being studied (the allocation rate or the number of eggs laid parasitically) is inherently monomorphic. This paper aims to explore the evolution of intra-specific brood parasitism without these restrictions. In the model, an individual is assigned a strategy, an allocation ratio of eggs that are laid parasitically in the nests of other individuals, and the strategy is inherited by offspring either asexually or sexually. Based on the simulation analysis, the evolution of the allocation rate (the extent of intra-specific brood parasitism) is discussed. The extension of this model to a tractable analytical model is also discussed.     

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.     

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.     

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.     

Paternity-parasitism trade-offs: a model and test of host-parasite cooperation in an avian conspecific brood parasite

Efforts to evaluate the evolutionary and ecological dynamics of conspecific brood parasitism in birds and other animals have focused on the fitness costs of parasitism to hosts and fitness benefits to parasites. However, it has been speculated recently that, in species with biparental care, host males might cooperate with parasitic females by allowing access to the host nest in exchange for copulations. We develop a cost-benefit model to explore the conditions under which such host-parasite cooperation might occur. When the brood parasite does not have a nest of her own, the only benefit to the host male is siring some of the parasitic eggs (quasi-parasitism). Cooperation with the parasite is favored when the ratio of host male paternity of his own eggs relative to his paternity of parasitic eggs exceeds the cost of parasitism. When the brood parasite has a nest of her own, a host male can gain additional, potentially more important benefits by siring the high-value, low-cost eggs laid by the parasite in her own nest. Under these conditions, host males should be even more likely to accept parasitic eggs in return for copulations with the parasitic female. We tested these predictions for American coots (Fulica americana), a species with a high frequency of conspecific brood parasitism. Multilocus DNA profiling indicated that host males did not sire any of the parasitic eggs laid in host nests, nor did they sire eggs laid by the parasite in her own nest. We used field estimates of the model parameters from a four-year study of coots to predict the minimum levels of paternity required for the costs of parasitism to be offset by the benefits of mating with brood parasites. Observed levels of paternity were significantly lower than those predicted under a variety of assumptions, and we reject the hypothesis that host males cooperated with parasitic females. Our model clarifies the specific costs and benefits that influence host-parasite cooperation and, more generally, yields precise predictions about expected levels of host male paternity. These predictions will enable a more rigorous assessment of field studies designed to test adaptive hypotheses of host-parasite cooperation.     

A brood parasite selects for its own egg traits

Many brood parasitic birds lay eggs that mimic their hosts'' eggs in appearance. This typically arises from selection from discriminating hosts that reject eggs which differ from their own. However, selection on parasitic eggs may also arise from parasites themselves, because it should pay a laying parasitic female to detect and destroy another parasitic egg previously laid in the same host nest by a different female. In this study, I experimentally test the source of selection on greater honeyguide (Indicator indicator) egg size and shape, which is correlated with that of its several host species, all of which breed in dark holes. Its commonest host species did not discriminate against experimental eggs that differed from their own in size and shape, but laying female honeyguides preferentially punctured experimental eggs more than host or control eggs. This should improve offspring survival given that multiple parasitism by this species is common, and that honeyguide chicks kill all other nest occupants. Hence, selection on egg size in greater honeyguides parasitizing bee-eaters appears to be imposed not by host defences but by interference competition among parasites themselves.     

Differential responses to related hosts by nesting and non-nesting parasites in a brood-parasitic duck

Host-parasite relatedness may facilitate the evolution of conspecific brood parasitism, but empirical support for this contention remains inconclusive. One reason for this disparity may relate to the diversity of parasitic tactics, a key distinguishing feature being whether the parasite has a nest of her own. Previous work suggests that parasites without nests of their own may be of inferior phenotypic quality, but because of difficulties in identifying these parasitic individuals, little is known about their host selection criteria. We used high-resolution molecular maternity tests to assign parasitic offspring to known parasites with and without their own nests in a population of Barrow's goldeneyes (Bucephala islandica). We determined whether parasite nesting status, host-parasite relatedness and distance between host and parasite nests affected the probability of parasitizing a host and the number of eggs laid per host. We also investigated whether nesting parasites, conventionally nesting females and non-nesting parasites differed regarding their age, structural size, body condition, nesting phenology or total brood size. The probability of engaging in parasitism increased with host-parasite relatedness and spatial proximity to host nests for nesting and non-nesting females alike. However, nesting parasites increased the number of eggs donated with relatedness to the host, while non-nesting parasites did not do so. Non-nesting parasites laid fewer eggs in total, but did not differ by any of the other quality measures from conventional nesters or nesting parasites. Our study provides the first demonstration that nesting and non-nesting parasites from the same population may use different host selection criteria.     

The optimal strategy for brood-parasitism: how many eggs should be laid in the host's nest?

We consider the optimal strategy for intra-specific brood-parasitism, especially with respect to the number of eggs laid by the parasitic individual in the nest of non-parasitic individual, in particular, a host that does not reject the parasite's eggs. With a fundamental mathematical model, assuming that the survival probability of the parasite's offspring in the nest of the host is significantly smaller than that in parasite's own nest, we determine the optimal number of eggs laid in the nest of host that maximizes the expected reproductive fitness of the parasite. We show that the invasion success of brood-parasitism could significantly depend on the total number of eggs laid by the parasite in a breeding season, and that the successfully invading brood-parasitism could realize maximum fitness with a specific number of parasite's eggs laid in the nest of the host.     

Size and material of model parasitic eggs affect the rejection response of Western Bonelli's Warbler Phylloscopus bonelli

Given the high costs of brood parasitism, avian hosts have adopted different defences to counteract parasites by ejecting the foreign egg or by deserting the parasitized nest. These responses depend mainly on the relative size of the host compared with the parasitic egg. Small hosts must deal with an egg considerably larger than their own, so nest desertion becomes the only possible method of egg rejection in these cases. The use of artificial model eggs made of hard material in egg‐recognition experiments has been criticized because hard eggs underestimate the frequency of egg ejection. However, no available studies have investigated the effect of softer material. Here, we test the potential effect of size of dummy parasitic eggs in relation to egg‐rejection behaviour (egg ejection and nest desertion rates) in Western Bonelli's Warbler Phylloscopus bonelli, a small host, using plasticine non‐mimetic eggs of three different sizes. In addition, we tested the potential effect of material, comparing ejection and desertion responses between real and plasticine eggs. As predicted, small eggs were always ejected, whereas nest desertion occurred more frequently with large eggs, thus suggesting that nest desertion occurs because of the constraints imposed by the large eggs. We found that plasticine may misrepresent the responses to experimental parasitism, at least in small host species, because this material facilitates egg ejection, provoking a decrease in nest desertion rate. Thus, particular caution is needed in the interpretation of the results in egg‐rejection experiments performed using dummy eggs made of soft materials.     

CLUTCH CHARACTERISTICS AND EGG DISCRIMINATIVE ABILITY OF THE AFRICAN VILLAGE WEAVERBIRD PLOCEUS CUCULLATUS

Over a three-year period, 917 eggs from 27 females were collected from a captive colony of African Village Weaverbirds Ploceus c. cucullatus. A study was made of egg-laying and incubation behaviour, clutch characteristics and egg recognition.
Fifteen yearling females laid their first clutches at a mean age of 348 days after hatching. The mean clutch-size was 2.26 in adults and 1.68 in yearlings. The mean clutch replacement interval was 6.6 days in adults and 7.4 days in yearlings with an absolute minimum of 4 days. Eggs were laid at intervals of from 24 to 26 hours beginning usually 2–3 hours after dawn.
The eggs laid by this species vary in ground colour and pattern of spotting between different females, but egg pigmentation is constant for each individual bird. The results of 322 egg-replacement tests showed that an individual female could recognise her own egg type and would eject from the nest eggs differing markedly from her own. The incidence of rejection was proportional the degree of difference between the eggs. The possible implications for parasitism by the Didric Cuckoo Chrysococcyx cuprius are discussed.     

Brood parasitism by cowbirds: risks and effects on reproductive success and survival in indigo buntings

We observed brood parasitism by brown-beaded cowbirds (Molothrusater) on indigo buntings (Passerina cyanea) and estimated dieimpact of parasitism on the success of the individual buntingsin their current nests and in their future survival and reproduction.Rates of parasitism over 8 years were 26.6% in 1040 nests and19.8% in 693 nests in two areas in southern Michigan. Risk ofparasitism was high early in the season; half the bunting nestswere begun after the end of the cowbird season. Risk was independentof female age, plant containing the nest, or habitat The immediatecost of parasitism was 1.19 and 1.26 fewer buntings fledgedper nest. Bunting success was lower in parasitized nests withcowbird eggs (nests were more likely to be deserted or predated),lower when the cowbird nestling failed (nests were more likelyto be predated), and lower when the cowbird fledged (fewer buntingsfledged) compared to nonparasitized nests. Costs were due toremoval of a bunting egg when die cowbird laid its own egg andto competition for parental care of the cowbird and buntingnestlings. Buntings that fledged from nests where a cowbirdalso fledged were only 18% as likely to survive and return totheir natal area in the next year as buntings from nests wherea cowbird did not fledge. Long-term effects of cowbird parasitismon adult breeding later in the season, survival to the nextseason, and reproductive success in the next season were negligiblewhen compared between birds that reared a cowbird and birdsthat reared only a bunting brood, or between birds that wereparasitized and birds that escaped parasitism. The results indicatelittle long-term cost of brood parasitism on individual fitnessof adult buntings beyond the impact on the current nest andthe survival of buntings that fledge from it; nearly all costis to the parasitized brood.     

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.     

Monogamy when there is potential for polygyny: tests of multiple hypotheses in a group-living fish

Monogamy within social groups where there exists a high potentialfor polygyny poses a challenge to our understanding of matingsystem evolution. Specifically, the traditional explanationthat monogamy evolves due to wide female dispersion, affordingmales little opportunity to defend multiple females, cannotapply. Instead, monogamy in groups potentially arises becausefemales compete for breeding resources such as breeding sites,food, and paternal care. We conducted manipulative experimentsto determine whether females compete over limiting resourceswithin groups of the obligate coral-dwelling goby, Paragobiodonxanthosomus (Gobiidae). Breeding females behaved aggressivelytoward individuals of their own sex and evicted subordinatefemales that were large and mature from the group. Experimentalremoval of nest sites caused breeding partners to breed in alternativenest sites, demonstrating that nest site limitation was notthe cause of female competition. Supplemental feeding resultedin an increase in the fecundity of breeding females but no maturationof subordinate females, demonstrating that food-limited femalefecundity was a likely cause of female competition. Finally,supplemental feeding of breeding pairs demonstrated that thedifference in eggs hatched by fed versus unfed males was lessthan the difference in eggs laid by fed versus unfed females,suggesting that paternal care limitation might also drive femalecompetition. These results suggest that competition over foodand possibly paternal care selects for dominant, breeding femalesto suppress the maturation of subordinate females to minimizecompetition. Monogamy in association with group living is thereforelikely to have evolved because female competition prevents malesfrom utilizing the potential for polygyny.     

Intraspecific nest parasitism and anti-parasite behavior in the grey starling,Sturnus cineraceus

I studied intraspecific nest parasitism in the grey starlingSturnus cineraceus in 1992 and 1993. The population in this study consisted of 290 nests (157 nests in 1992 and 133 nests in 1993) in which the clutches were completed before May 10 in the year studied. Twenty-nine nests in 1992 and 32 nests in 1993 contained at least 1 parasitic egg. Hatching success per nest of parasitized nests was slightly higher than that of non-parasitized nests. However, fledging success per nest of parasitized nests was significantly lower than that of non-parasitized nests. Thus parasitism appeared to reduce the reproductive success of hosts. Hosts exhibited a few behaviors that minimized the potential cost of brood parasitism. These behaviors included throwing out the parasitic egg and nest guarding. Hosts threw out parasitic eggs before the onset of laying, but they never did so to parasitic eggs laid after that period. The nest guarding level was low during the hosts’ laying periods, and one observed nest was parasitized during this time. Thus, nest-guarding behavior was not effective as an anti-parasite behavior. Grey starlings do not appear to adopt strategies effective in reducing parasitism.     

Egg removal by cuckoos forces hosts to accept parasite eggs

Many avian brood parasites remove one or more host eggs before laying their own eggs in the host nest. Various hypotheses have been proposed to explain the adaptive significance of this behaviour, but none of them provides an adequate explanation. Here we provide a new hypothesis for explaining why a parasite removes host eggs before laying its own. In this study, we attempted to answer this question by constructing a mathematical model that focused on the changes in host decision making according to reduced clutch size as a consequence of egg removal by parasites. We assume that a host selects one of the following two options to maximise the number of its own chicks: trying to eject a suspicious egg from the nest (trying‐to‐eject) or acceptance without trying to eject the egg (acceptance). The option selected depends on the number of eggs in the nest. Our model provides a new explanation for egg removal behaviour by showing that the host should select trying‐to‐eject if there is a large number of eggs in the nest but acceptance with a small number of eggs. This is because the relative payoff for a host that selects trying‐to‐eject decreases with the number of eggs in the nest. Therefore, parasites benefit by removing the host egg because this behaviour reduces the number of eggs in the nest, thereby increasing the probability of their own eggs being accepted. Thus, hosts have evolved egg ejection to combat brood parasites, but it may also have facilitated the evolution of egg removal by parasites. This hypothesis may also apply to brood parasitic species that do not eject host chicks. In addition, this hypothesis may explain other parasitic behaviours, such as egg damaging and egg puncturing, which lead to reductions in the host clutch size.     

Why do snow geese adopt eggs?

Nesting female lesser snow geese (Anser caerulescens caerulescens)usually adopt eggs that are laid adjacent to their nests bypotential intraspecific nest parasites. The host female rollsthe parasite’s egg up into the nest, using the same behaviorpatterns used to retrieve her own eggs if they are displacedfrom the nest. The reproductive consequences of adopting eggsare unclear. We consider three selective scenarios that mightmaintain adoption behavior in geese: (1) egg adoption is ofno reproductive consequence to the host; (2) egg adoption augmentshost reproductive success relative to that of unparasitizednests; and (3) egg adoption is making the best of a bad situation,once a female’s options are constrained by the presenceof an egg adjacent to the nest; we also consider (4) the possibilitythat adoption, if not concordant with the selective regime,is maladaptive. Nest parasitism is costly to the host, makinghypotheses 1 and 2 unlikely. However, adopting eggs significantlydecreases the risk of total nest failure during laying, morethan offsetting other probable host costs. This is consistentwith hypothesis 3. Experiments show that geese have limitedabilities to retrieve eggs, which accounts for most cases ofnonadoption of nearby eggs. We conclude that adoption of eggsis an adaptive trait, a form of nest protection. Adopting eggsis the best option within the species’ repertoire to thethreat to nest survival created when a parasite lays an eggnext to the nest. [Behav Ecol 1991;2:181-187]     

Intraspecific nest parasitism in the Spotless Starling Sturnus unicolor

Intraspecific nest parasitism in two colonies of Spotless Starling Sturnus unicolor breeding in nestboxes was studied in central Spain from 1991 to 1994. Nests were monitored regularly and three criteria were used to detect nest parasitism: the appearance of more than one egg per day during the laying period of the host; the appearance of an egg after the start of incubation; eggs with unusual shape or pigmentation. The proportion of parasitized nests in first clutches (37%) was twice that of intermediate (19%) or second (20%) clutches in colony B, whereas parasitism occurred in first (35%) and intermediate (12%) but not in second clutches in colony A. Most clutches (52–70%) were parasitized during the host's laying period and received one parasitic egg. In 10% of the parasitized clutches in colony B, one of the host's eggs disappeared on the day the parasitic egg was added, suggesting that the parasitic female removed this egg. Although parasitism increased clutch size significantly, it led to a decrease in host breeding success, mainly through the removal of eggs and the loss of host nestlings and the survival of parasitic chicks. Observations suggested that parasitic females were young individuals without their own nests and/or those whose breeding attempt had been disrupted while laying in their own nest.     

Nest destruction elicits indiscriminate con‐ versus heterospecific brood parasitism in a captive bird

Following nest destruction, the laying of physiologically committed eggs (eggs that are ovulated, yolked, and making their way through the oviduct) in the nests of other birds is considered a viable pathway for the evolution of obligate interspecific brood parasitism. While intraspecific brood parasitism in response to nest predation has been experimentally demonstrated, this pathway has yet to be evaluated in an interspecific context. We studied patterns of egg laying following experimental nest destruction in captive zebra finches, Taeniopygia guttata, a frequent intraspecific brood parasite. We found that zebra finches laid physiologically committed eggs indiscriminately between nests containing conspecific eggs and nests containing heterospecific eggs (of Bengalese finches, Lonchura striata vars. domestica), despite the con‐ and heterospecific eggs differing in both size and coloration. This is the first experimental evidence that nest destruction may provide a pathway for the evolution of interspecific brood parasitism in birds.     

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.