Host-parasite Relatedness Research Articles

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 492m from their previous year's nest site, while successful females only moved an average of 13m. 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.

Helping Relatives Survive and Reproduce: Inclusive Fitness and Reproductive Value in Brood Parasitism.

Costly help can raise a relative's reproduction, survival, and reproductive value and increase the inclusive fitness of the donor of help. Donor fitness is explored here in conspecific brood parasitism. In this alternative reproductive tactic, some females, "parasites," lay eggs in nests of other females of the same species, "hosts," suppliers of help that alone take care of the offspring. Modeling shows that hosts can gain inclusive fitness if parasitized by relatives whose reproduction or survival is thereby increased. These predictions are explored in waterfowl with frequent brood parasitism, female-biased philopatry, and neighbor relatedness. Approximate estimates based on waterfowl reproductive and life-history data show that host inclusive-fitness gain is often possible with related parasites. The largest gains can be achieved through increased reproduction, but gain is also possible through higher survival of parasites that avoid increased predation and other risks of nesting. Inclusive fitness depends on parasite reproductive value and can be highest for a host parasitized by her mother and for old, senescent hosts with low fecundity, helping young related parasites. These results and observed levels of host-parasite relatedness suggest that being "parasitized" in waterfowl is sometimes neutral or even advantageous because of inclusive-fitness benefits, contributing to evolution of frequent conspecific brood parasitism in this group.

Kin-biased conspecific brood parasitism in a native Mandarin duck population

Conspecific brood parasitism (CBP) is a widespread female alternative reproductive tactic, where clutches tended by a single female contain eggs laid by different females. CBP is disproportionately common in waterfowl, where females, not males, exhibit natal philopatry. This raises the possibility that closely related females cooperate with each other for inclusive fitness benefits and may explain why females expend effort raising offspring that are not their own. Some studies show higher host–parasite relatedness than expected, while a similar number of studies fail to do so. Here we test the hypothesis that host and parasite are closely related in Mandarin ducks (Aix galericulata) to further our understanding of the role of host–parasite relatedness in the evolution of CBP. Using microsatellite markers, we found that more than 33.7 % of ducklings were parasites and that more than 70 % of nests contained parasitic offspring. Relatedness between host mother and parasitic ducklings was significantly higher than that of host mothers and ducklings in other nests, showing hosts were, on average, more related to their parasites than to other breeding females. There was a weak negative relationship between pairwise relatedness and distance between nests. However, distance did not contribute to the higher relatedness of host and parasite. Thus, host–parasite relatedness likely involved some form of kin recognition. Based on our results, relatedness plays a role in CBP in Mandarin ducks, though the explicit fitness benefits to both the host and the parasite still need to be determined.

Female sociality and kin discrimination in brood parasitism: unrelated females fight over egg laying

In conspecific brood parasitism, some females (“parasites”) lay eggs in nests of other females of the same species (“hosts”). This reproductive tactic is particularly common in waterfowl, in which studies suggest that parasites are often related to the host. Here, we test the hypothesis that hosts may discriminate and reject unrelated parasites. Based on observations and >4100h of digital video film, we analyze behavioral interactions at 65 nests of High Arctic common eiders during the laying sequence. We also estimate parasitism and host–parasite relatedness by albumen fingerprinting of 975 eggs from 232 nests. Among the video-filmed nests in which interactions were recorded during the egg-laying period, 11 had eggs from 2 females. At 8 of these 11 nests, there was overt female aggression and significantly lower host–parasite relatedness (mean coefficient of relationship r = −0.40) than in the nests with tolerant or no interactions (r = 0.91). The results demonstrate active female kin discrimination in common eiders, used against nonrelatives that try to lay eggs in the nest. Other females trying to access the nest were often prevented from doing so: in 65% of 34 such attempts, the sitting female rejected the intruder. Brood “parasitism” in eiders and other waterfowl is complex, ranging from violent female conflict and parasitic exploitation of the host’s parental care to nest takeover and potential kin selection favoring acceptance of related parasites. These and other aspects of female sociality in eiders are discussed; in some respects, they may resemble certain long-lived matriarchal mammals.

Co-parasites preferentially lay with kin and in safe neighbourhoods: experimental evidence from goldeneye ducks

Conspecific brood parasitism (CBP) is an alternative reproductive tactic in several animal taxa. Recently the role of kinship in CBP has been in focus, and some studies have demonstrated high host–parasite relatedness in avian CBP systems. However, high natal and breeding site fidelity of hosts and parasites complicates the interpretation of previous observational findings, and the mechanisms leading to high host–parasite relatedness remain unknown. Some recent findings suggest that broadening the scope of the study of interactions may cast light on these mechanisms. We studied relatedness between parasites laying in the same nest (co-parasites) and factors possibly driving relatedness patterns between co-parasites in the common goldeneye, Bucephala clangula. Based on a field experiment, controlling for site fidelity and host role, we report here that both relatedness and safety of the nest site, and their interaction, affected the likelihood of two females engaging in co-parasitism. At the population level, parasites indeed seemed to lay eggs preferentially with kin. Analyses at a finer spatial scale revealed that high relatedness between co-parasites was not due to the philopatry effect only. Parasites engaging in co-parasitism also laid in safer neighbourhoods than parasites that did not engage in co-parasitism; the number of nondepredated nesting attempts the previous year was higher for the parasites engaging in co-parasitism. However, the interaction between relatedness and safety of the nest site suggests that co-parasitism at dangerous lakes was more likely to involve relatives. Our results provide the first experimental evidence that nest predation risk and interaction between related parasites are associated with kin-biased co-parasitism in a CBP system.

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.

Relatedness and spatial proximity as determinants of host–parasite interactions in the brood parasitic Barrow's goldeneye (Bucephala islandica)

Recent studies, which have found evidence for kin-biased egg donation, have sparked interest in re-assessing the parasitic nature of conspecific brood parasitism (CBP). Since host-parasite kinship is essential for mutual benefits to arise from CBP, we explored the role of relatedness in determining the behaviour of conspecific nest parasites and their hosts in nesting female Barrow's goldeneyes (Bucephala islandica), a duck in which CBP is common. The results revealed that the amount of parasitism increased with host-parasite relatedness, the effect of which was independent of geographical proximity of host and parasite nests. Proximity per se was also positively associated with the amount of parasitism. Furthermore, while hosts appeared to reduce their clutch size as a response to the presence of parasitic eggs, the magnitude of host clutch reduction also tended to increase with increasing relatedness to the parasite. Hence, our results indicate that both relatedness and spatial proximity are important determinants of CBP, and that host clutch reduction may be an adaptation to nest parasitism, modulated by host-parasite relatedness. Taken together, the results provide a demonstration that relatedness influences host and parasite behaviour in Barrow's goldeneyes, resulting in kin-biased egg donation.

Spatial relatedness and brood parasitism in a female-philopatric bird population

The spatial structure of relatedness between individuals in a population can be crucial for social selection and evolution. Here we analyze a female alternative reproductive tactic, conspecific brood parasitism, in relation to spatial relatedness among females in a Baltic Sea population of the common eider Somateria mollissima. The role of relatedness in brood parasitism is debated: some models predict parasite avoidance of related hosts, others predict host–parasite relatedness. We estimate pairwise relatedness from protein fingerprinting of egg albumen in 156 nests, with pairwise nest distances ranging from 1 to 6 km. Relatedness increases significantly from the longest distances to an average of r ’ 0.09 below 20 m. Brood parasitism is common, and average pairwise relatedness between host and parasite is estimated at 0.18–0.21. Parasites thus do not avoid relatives, and combined with the findings of a similar study in another eider population, the results show that mean host–parasite relatedness is higher than that among close neighbors. High host–parasite relatedness is therefore not an effect of natal philopatry alone; some other form of kin bias is also involved. Recognition and association between birth nest mates is a candidate mechanism for further study. Key words: joint nesting, kinship, local genetic structure, protein fingerprinting, spatial trend analysis. [Behav Ecol]

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.

Host-parasite relatedness in wood ducks: patterns of kinship and parasite success

We investigated the role of kinship in intraspecific nest parasitism of wood ducks (Aix sponsa). Among waterfowl, female philopatry creates the potential for female relatives to nest in proximity. Costs of intraspecific nest parasitism to host females may be reduced if parasites lay eggs with kin. However, previous observations of marked wood ducks indicated that females avoided parasitizing clutch mates or the female that incubated them. To further examine the role of kinship, we determined the genotypes of 27 host-parasite pairs at five microsatellite loci. Average relatedness between hosts and all females laying parasitic eggs was only 0.04 6 0.03. Parasites appeared to choose hosts randomly with respect to kinship from among females with nests in the neighborhood and those within the entire study area. However, host relatedness to the parasite with the greatest number of young leaving the nest was 0.11 6 0.03, which was greater than expected if eggs were accepted randomly from neighboring females or from females present on the entire study area (p ¼ .03 and p ¼ .02, respectively). These patterns may reflect parasitism of randomly selected nests followed by differential acceptance by hosts, differential hatching success of related parasites (e.g., due to greater laying synchrony), or a mixture of parasitic strategies, one with a focus on related hosts and the other on unrelated hosts. Genetic data revealed that social relationships did not always reflect true relatedness and that success of primary parasites was associated with kinship to hosts. Key words: Aix sponsa, intraspecific nest parasitism, kin selection, microsatellites, relatedness, wood ducks. [Behav Ecol]

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.

Low host recognition tendency revealed by experimentally induced parasitic egg laying in the common goldeneye (Bucephala clangula)

Host-parasite relatedness has been suggested to promote the evolution of conspecific brood parasitism, an alternative reproductive tactic pursued by females in several animal taxa. An essential prerequisite for relatedness to promote brood parasitism is accurate kin recognition, including the recognition of related hosts by parasites. I performed a field experiment to address the accuracy of host recognition by parasites in the common goldeneye (Bucephala clangula), a cavity-nesting duck. I studied whether parasites discriminate between experimental nests that did not have a host (i.e., new nest boxes that contained chicken eggs dyed to mimic the colour of common goldeneye eggs) and real nests that did have a host (i.e., active nests that progressed to incubation). Parasitic egg laying in the experimental nests was not constrained by the lack of contemporarily available nests that had a host; it was also not constrained by the lack of suitable and empty nest sites. There was no difference in the start of parasitic laying between the experimental and real nests. The experimental nests and real nests were equally parasitized. The findings suggest that host recognition by parasites is not sophisticated in the common goldeneye, questioning the possible function of accurate kin recognition in brood parasitism in this species.

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.

Host-parasite relatedness shown by protein fingerprinting in a brood parasitic bird.

Brood parasitism as an alternative female breeding tactic is particularly common in ducks, where hosts often receive eggs laid by parasitic females of the same species and raise their offspring. Herein, we test several aspects of a kin selection explanation for this phenomenon in goldeneye ducks (Bucephala clangula) by using techniques of egg albumen sampling and statistical bandsharing analysis based on resampling. We find that host and primary parasite are indeed often related, with mean r = 0.13, about as high as between first cousins. Relatedness to the host is higher in nests where a parasite lays several eggs than in those where she lays only one. Returning young females parasitize their birth nestmates (social mothers or sisters, which are usually also their genetic mothers and sisters) more often than expected by chance. Such adult relatives are also observed together in the field more often than expected and for longer periods than other females. Relatedness and kin discrimination, which can be achieved by recognition of birth nestmates, therefore play a role in these tactics and probably influence their success.