Phenotypic variation in nestlings of a bird of prey under contrasting breeding and diet conditions

Environmental conditions often vary in space and time, and this may explain variation in the expression of phenotypic traits related to individual quality, such as ornamental coloration. Furthermore, the direction and strength of the relationship between coloured trait expression and individual quality might vary under contrasting conditions. These issues have been explored in adult birds but much less so in nestlings, which are more likely to experience different selective pressures and different physiological trade‐offs than adults. Here, we empirically investigated the effects of contrasting breeding and diet conditions on the expression of carotenoid‐based colour traits displayed by marsh harrier (Circus aeruginosus) nestlings. We studied the variation in coloration, body condition, and immune responsiveness of nestlings in four populations over a 5‐year period. We characterized spatiotemporal differences in rearing conditions experienced by C. aeruginosus nestlings in terms of breeding (laying date, clutch size, and number of nestlings hatched and fledged) and diet (percentage of mammal in diet and prey diversity) conditions. We found that breeding conditions influenced the co‐variation between coloration and immune responsiveness in female nestlings, and that diet conditions influenced the condition‐dependence of nestling coloration in later‐hatched nestlings. In addition, breeding conditions influenced nestling body condition and immune responsiveness, whereas diet conditions influenced nestling coloration and body condition. Our study highlights that nestling phenotype (levels of signalling, circulating carotenoids, and immunity) varies both spatially and temporally, and that some of this variation is related to differences in breeding and diet conditions. Moreover, under contrasting conditions, the direction of the relationships between nestling carotenoid‐based coloration and nestling quality may also vary. In order to fully understand the evolution and maintenance of colour traits in nestling birds, studies and experiments should ideally be replicated under contrasting rearing conditions. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

Brood size manipulations reveal relationships among physiological performance,body condition and plumage colour in Northern Flicker Colaptes auratus nestlings

Visual signals of quality in offspring, such as plumage colour, should honestly advertise need and/or body condition, but links between nutritional status, physiological performance and the expression of colours are complex and poorly understood. We assess how food stress during rearing affected two physiological measures (T‐cell‐mediated immune function and corticosterone level in feathers: CORT_f) and how these two variables were related to carotenoid and melanin coloration in Northern Flicker Colaptes auratus nestlings. We were also interested in how these two physiological measures were influenced by the sex of the nestling. We experimentally manipulated brood size to alter levels of food availability to nestlings during development. We measured carotenoid‐based colour (chroma and brightness) in wing feathers and the size of melanin spots on breast feathers. In agreement with our prediction, nestlings in the reduced brood treatment had better body condition and stronger immune responses than those in the control and brood enlargement treatments. This supports the hypothesis that immune responses are energetically costly. In contrast, CORT_f was not related to nestling body condition or sex and was unaffected by brood size manipulation. Nestlings of both sexes with stronger T‐cell‐mediated immune responses had larger melanin spots but only males with higher immune responses also had brighter flight feathers. Feather brightness decreased with increasing CORT_f levels. Our study is one of the few to examine the relationship between multiple physiological and plumage measures in nestlings and shows that plumage colour and immune function signalled body condition of nestlings, but that feather corticosterone levels did not.     

Sex and testosterone effects on growth, immunity and melanin coloration of nestling Eurasian kestrels

1. Sex differences in testosterone levels and sex-biased sensitivity to testosterone are the basis of some ideas postulated to account for sex-linked environmental vulnerability during early life. However, sex variation in circulating testosterone levels has been scarcely explored and never manipulated at post-natal stages of birds in the wild. 2. We measured and experimentally increased circulating testosterone levels in nestling Eurasian kestrels Falco tinnunculus. We investigated, possible sexual differences in testosterone levels and the effect of this hormone on growth (body mass and tarsus length) and cell-mediated immunity in males and females. We also explored testosterone effects on rump coloration, a highly variable melanin-based trait in male nestlings. We analysed data on circulating testosterone levels of nestlings in 15 additional bird species. 3. Increased levels of testosterone tended to negatively affect body condition, reduced cell-mediated immune responses in male and female nestlings and also diminished the expression of grey rump coloration in male nestlings. No sex differences were observed in testosterone levels in either control or increased testosterone group nestlings, and no interactions were found between sex and treatment. However, male nestlings showed a lower cell-mediated immune response than females in both groups. 4. Our results indicate first, that a high level of testosterone in all nestlings in a brood entails costs, at least in terms of immunity, coloration and probably growth. Secondly, sex differences in post-natal cell-mediated immunity, and consequently in the capacity to prevent diseases, cannot be explained by sex differences in circulating testosterone levels. Finally, by comparing published data at an interspecific level, contradictory sex patterns in circulating testosterone levels have been found, supporting the idea that circulating testosterone might not be a proximate factor causing sex-dependent vulnerability in bird species.     

Hatching asynchrony and brood reduction influence immune response in Common Kestrel Falco tinnunculus nestlings

The onset of incubation before the end of laying imposes asynchrony at hatching and, therefore, a size hierarchy in the brood. It has been argued that hatching asynchrony might be a strategy to improve reproductive output in terms of quality or quantity of offspring. However, little is known about the mediating effect of hatching asynchrony on offspring quality when brood reduction occurs. Here, we investigate the relationship between phenotypic quality and hatching asynchrony in Common Kestrel Falco tinnunculus nestlings in Spain. Hatching asynchrony did not increase breeding success or nestling quality. Furthermore, hatching asynchrony and brood reduction had different effects on nestlings’ phytohaematogglutinin (PHA)‐mediated immune response and nestling growth. In asynchronous and reduced broods (in which at least one nestling died), nestlings showed a stronger PHA‐mediated immune response and tended to have a smaller body size compared with nestlings raised in synchronous and reduced broods. When brood reduction occurred in broods hatched synchronously, there was no effect on nestling size, but nestlings had a relatively poor PHA‐mediated immune response compared with nestlings raised in asynchronous and reduced broods. We suggest that resources for growth can be directed to immune function only in asynchronously hatched broods, resulting in improved nestling quality, as suggested by their immune response. We also found that males produced a greater PHA‐mediated immune response than females only in brood‐reduced nests without any effect on nestling size or condition, suggesting that females may trade off immune activities and body condition, size or weight. Overall, our results suggest that hatching pattern and brood reduction may mediate resource allocation to different fitness traits. They also highlight that the resolution of immune‐related trade‐offs when brood reduction occurs may differ between male and female nestlings.     

Influence of hatching asynchrony and within-brood parental investment on size, condition, and immunocompetence in nestling red-billed choughs

Studies of hatching asynchrony have rarely assessed the effect of parental investment strategies on the development of intra-brood hierarchies using indicators of nestling quality. The influence of hatching asynchrony and other variables related to parental investment on immunocompetence was evaluated measuring T-cell mediated immune response in broods of red-billed choughs ( Pyrrhocorax pyrrhocorax ), a large long-living passerine with a pronounced sexual size dimorphism. The results showed that T-cell mediated immune response depends on parental effects as shown by the differences between broods on hatching asynchrony. Male nestlings were both heavier and larger than female nestlings, but there was no effect of hatching order on these traits, nor on sex differences in immunocompetence. Differential investment strategy in relation to laying order did not favour older offspring or either of the sexes. Successful reproduction in this species might be so unpredictable and infrequent that strategies of parental investment in the brood could have evolved to attempt to maximize the survival of all nestlings by avoiding within-brood hierachies of size, body condition, and immunocompetence.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 675–684.     

Immune function and survival of great tit nestlings in relation to growth conditions

Life history theory predicts a trade-off between number and quality of offspring. Reduced quality with increasing brood size may arise from a decrease in body condition or in immunocompetence that would be important in fighting off virulent parasites by immunologically naive offspring. We tested the effect of rearing conditions on immune function of nestling great tits (Parus major) by reducing or increasing broods by two hatchlings. In the middle of the nestling period (on day 8), nestlings from enlarged broods developed lower T cell responses [as measured from the cutaneous swelling reaction to injection with phytohaemagglutinin (PHA)] and tended to have lower total leukocyte and lymphocyte concentrations in their peripheral blood than nestlings from reduced broods. Brood size manipulation affected the PHA response of nestlings most strongly in small clutches, suggesting that nestling immune function was dependent on their parents’ condition, as estimated by original clutch size. Intra-brood differences in nestling mortality were unrelated to immune parameters, but nestlings in broods without mortality had a stronger PHA response, higher concentration of lymphocytes and higher body mass on day 15 than nestlings in broods with mortality. These results support the prediction that the immune function of altricial birds is affected by rearing conditions, and that growth and immune parameters are related to inter-brood differences in nestling survival. Received: 1 February 1999 / Accepted: 19. July 1999     

Synergistic and antagonistic interaction between different branches of the immune system is related to melanin‐based coloration in nestling tawny owls

When exposed to parasites, hosts often mount energetically expensive immune responses, and this may alter resource allocation between competing life history traits including other components of the immune system. Here, we investigated whether a humoral immune challenge towards a vaccine reduces or enhances the cutaneous immune responses towards an injection of lipopolysaccharid (LPS, innate immunity) and phytohaemagglutinin (PHA, T‐cell immunity) in nestling tawny owls in interaction with the degree of plumage melanin‐based coloration. The humoral immune challenge enhanced the response to LPS similarly in differently coloured nestlings. In contrast, the same humoral immune challenge enhanced immune response to PHA in dark reddish melanic nestlings while reducing it in pale reddish melanic nestlings. Our results highlight that both antagonistic and synergistic interactions can take place among branches of immune system, and that the sign and magnitude of these interactions can vary with immune responses involved and the degree of melanin‐based coloration.     

Rearing environment effects on immune defence in blue tit Cyanistes caeruleus nestlings

Rearing conditions may influence ontogeny and functioning of the immune system. Activation of different mechanisms involved in host disease resistance and their internal regulation can be affected by intrinsic and extrinsic factors influencing development. I investigated how rearing environment can influence associations between humoral and cellular constituents of immune defence in nestling blue tits (Cyanistes caeruleus). The ability to mount a cell-mediated immune response was estimated as a hypersensitivity reaction to phytohaemagglutinin, and the ontogeny of humoral immunity was determined by assessing circulating levels of total IgG in 15-day-old nestlings. Heterogeneity in rearing conditions was evoked by placing nest-boxes in areas differing in habitat structural characteristics, and examining natural variation in nest ectoparasite infestations, hatching date, brood size and brood sex-ratio. Habitat characteristics, parasitism and hatching date may shape associations between different components of the immune system in developing birds. I discuss the effects of rearing conditions on the interaction between different arms of the immune system and the implications for understanding negative correlations within the immune system at the individual and brood level.     

Context‐dependent effects of yolk androgens on nestling growth and immune function in a multibrooded passerine

Female birds may adjust their offspring phenotype to the specific requirements of the environment by differential allocation of physiologically active substances into yolks, such as androgens. Yolk androgens have been shown to accelerate embryonic development, growth rate and competitive ability of nestlings, but they can also entail immunological costs. The balance between costs and benefits of androgen allocation is expected to depend on nestling environment. We tested this hypothesis in a multibrooded passerine, the spotless starling, Sturnus unicolor. We experimentally manipulated yolk androgen levels using a between‐brood design and evaluated its effects on nestling development, survival and immune function. Both in first and replacement broods, the embryonic development period was shorter for androgen‐treated chicks than controls, but there were no differences in second broods. In replacement broods, androgen‐treated chicks were heavier and larger than those hatched from control eggs, but this effect was not observed in the other breeding attempts. Androgen exposure reduced survival with respect to controls only in second broods. Regarding immune function, we detected nonsignificant trends for androgen treatment to activate two important components of innate and adaptive immunity (IL‐6 and Ig‐A levels, respectively). Similarly, androgen‐treated chicks showed greater lymphocyte proliferation than controls in the first brood and an opposite trend in the second brood. Our results indicate that yolk androgen effects on nestling development and immunity depend on the environmental conditions of each breeding attempt. Variation in maternal androgen allocation to eggs could be explained as the result of context‐dependent optimal strategies to maximize offspring fitness.     

Parasites favour intermediate nestling mass and brood size in cliff swallows

A challenge of life‐history theory is to explain why animal body size does not continue to increase, given various advantages of larger size. In birds, body size of nestlings and the number of nestlings produced (brood size) have occasionally been shown to be constrained by higher predation on larger nestlings and those from larger broods. Parasites also are known to have strong effects on life‐history traits in birds, but whether parasitism can be a driver for stabilizing selection on nestling body size or brood size is unknown. We studied patterns of first‐year survival in cliff swallows (Petrochelidon pyrrhonota) in western Nebraska in relation to brood size and nestling body mass in nests under natural conditions and in those in which hematophagous ectoparasites had been removed by fumigation. Birds from parasitized nests showed highest first‐year survival at the most common, intermediate brood‐size and nestling‐mass categories, but cliff swallows from nonparasitized nests had highest survival at the heaviest nestling masses and no relationship with brood size. A survival analysis suggested stabilizing selection on brood size and nestling mass in the presence (but not in the absence) of parasites. Parasites apparently favour intermediate offspring size and number in cliff swallows and produce the observed distributions of these traits, although the mechanisms are unclear. Our results emphasize the importance of parasites in life‐history evolution.     

An analysis of pre- and post-hatching maternal effects mediated by carotenoids in the blue tit

Maternal effects increase phenotypic plasticity in offspring traits and may therefore facilitate adaptation to environmental variability. Carotenoids have been hypothesized to mediate costs of reproduction in females as well as maternal effects. However, assessing potential transgenerational and population consequences of environmental availability of carotenoids requires a better understanding of mechanisms of maternal effects mediated by these antioxidant pigments. Manipulating dietary availability of carotenoids to egg-laying female blue tits and subsequently cross-fostering nestlings between female treatments allowed us to specifically investigate the relative importance of maternal effects through egg carotenoids and through post-hatching care mediated by antioxidants in females. Nestling body size and mass and plasma antioxidants were not significantly affected by pre- or post-hatching maternal effects mediated by antioxidants, although both types of maternal effects in interaction explained the variation in growth, as measured by wing length. Development of the ability to mount a cell-mediated immune response as well as its temporal dynamics was influenced by both pre- and post-hatching maternal effects, with an advantage to nestlings originating from, or reared by, carotenoid-supplemented females. In addition, nestlings reared by carotenoid-fed females had a lower blood sedimentation rate, indicating that they may have been less infected than nestlings from controls. Finally, prehatching maternal effects in interaction with nestling plasma carotenoid levels affected the development of carotenoid-based plumage. Maternal effects mediated by carotenoids may thus act as a proximate factor in development and phenotypic plasticity in traits associated with nestling fitness, such as immune response and ability to metabolize and use antioxidants, and ultimately participate in the evolution of phenotypic traits.     

Secondary phytohaemagglutinin (PHA) swelling response is a good indicator of T‐cell‐mediated immunity in free‐living birds

The validity of using the phytohaemagglutinin (PHA) test to measure acquired immunity, one of the most widely used methods, is currently being debated due to new knowledge on the complex physiology of the process. As a greater secondary response to repeated challenges linked to increases of circulating lymphocyte levels would be indicative of a T‐cell‐mediated immune response, we performed for the first time an experiment under natural conditions with repeated PHA challenges in free‐living adult birds and chicks to shed light on this topic. We found significantly stronger secondary response to PHA injection independent of sex or age, while controlling for body condition, the second response being on average 90% larger than the first. Likewise, lymphocyte counts were significantly higher in the second PHA challenge, whereas no significant differences were found among untreated birds. Significant positive correlations between the PHA response and both lymphocyte counts and plasma protein levels (mainly albumin, globulin precursor) were recovered, whereas no significant differences were recovered in plasma protein levels between challenges. Our results are consistent with those from captive birds, supporting the validity of the PHA skin‐swelling test as an accurate gauge of acquired T‐cell‐mediated immunity in birds.     

Host tolerance and resistance to parasitic nest flies differs between two wild bird species

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Nest size predicts the effect of food supplementation to magpie nestlings on their immunocompetence: an experimental test of nest size indicating parental ability

Post-mating sexually selected signals are expected to indicateparental quality. The good parent model assumes that expressionof the sexual character positively reflects parental ability,resulting in a potential link between the exaggeration of thecharacter and nestling-fitness traits. We tested this predictionin a population of a monogamous passerine, the magpie (Picapica), for which nest size is known to act as a post-matingsexually selected signal. We provided a food supplement to halfof the magpie nestlings in each nest, keeping the other halfas control nestlings. We found that food-supplemented nestlingsexperienced a significantly higher T-cell-mediated immune responseand a tendency to an increased condition index. In accordancewith the good parent model, we found that nest size was positivelyrelated to T-cell mediated immune response for control magpie,whereas this relationship was nonexistent in food-supplementednestlings. In addition, the difference in T-cell mediated immuneresponse between food-supplemented and control nestlings ofthe same nest was principally explained by nest size. Basedon our results, we discuss that magpie pairs with large nestsprovided their nestlings with higher quality food as comparedto pairs with smaller nests, nest size thereby being an indicatorof parental ability. To our knowledge, this is the first studyshowing a link between a post-mating sexually selected signaland nestling immunocompetence, a trait closely related to fitnessin birds.     

Are Maternal Antibodies Really That Important? Patterns in the Immunologic Development of Altricial Passerine House Sparrows (Passer domesticus)

Background

Maternal antibodies are believed to play an integral role in protecting immunologically immature wild-passerines from environmental antigens. This study comprehensively examines the early development of the adaptive immune system in an altricial-developing wild passerine species, the house sparrow (Passer domestics), by characterizing the half-life of maternal antibodies in nestling plasma, the onset of de novo synthesis of endogenous antibodies by nestlings, and the timing of immunological independence, where nestlings rely entirely on their own antibodies for immunologic protection.

Methodology/Principal Findings

In an aviary study we vaccinated females against a novel antigen that these birds would not otherwise encounter in their natural environment, and measured both antigen-specific and total antibody concentration in the plasma of females, yolks, and nestlings. We traced the transfer of maternal antibodies from females to nestlings through the yolk and measured catabolisation of maternal antigen-specific antibodies in nestlings during early development. By utilizing measurements of non-specific and specific antibody levels in nestling plasma we were able to calculate the half-life of maternal antibodies in nestling plasma and the time point at which nestling were capable of synthesizing antibodies themselves. Based on the short half-life of maternal antibodies, the rapid production of endogenous antibodies by nestlings and the relatively low transfer of maternal antibodies to nestlings, our findings suggest that altricial-developing sparrows achieve immunologic independence much earlier than precocial birds.

Conclusions/Significance

To our knowledge, this is the first in depth analyses performed on the adaptive immune system of a wild-passerine species. Our results suggest that maternal antibodies may not confer the immunologic protection or immune priming previously proposed in other passerine studies. Further research needs to be conducted on other altricial passerines to determine if the results of our study are a species-specific phenomenon or if they apply to all altricial-developing birds.     

Immunological development in nestling American kestrels Falco sparverius: post-hatching ontogeny of the antibody response

Avian research involving examination of immune function or testing of immunocompetence in wild birds has been based upon information on Galliforms, (chicken and quail) even though they are precocial, whereas most wild species with which ecologists, biologists and toxicologists work are altricial; blind, naked and completely dependent at hatching. Here we begin to address this gap in knowledge, offering insight into the early, post-hatching, humoral immune response in an altricial bird, the American kestrel (Falco sparverius). Over two breeding seasons, nestling kestrels were immunized with a non-pathogenic antigen, dinitrophenol keyhole limpet hemocyanin (DNP-KLH), between 3 and 9 days post-hatching and boostered 6 days later. Background levels, primary and secondary immune responses were measured using an enzyme linked immunosorbent assay. The specificity of our laboratory produced rabbit, anti-kestrel antibody was determined using a double immunodiffusion assay. Results showed the rabbit antiserum to have specific anti-kestrel IgG activity. Birds as young as three days old could successfully mount an antibody response, the magnitude of which increased with age at first vaccination. Early immunization did not compromise growth rate, nor did it affect the maximum secondary response. Comparatively, adult kestrels immunized during the same season and following the same protocol, had antibody levels four times higher than those of the nestlings.     

Rejection of brood‐parasitic shiny cowbird Molothrus bonariensis nestlings by the firewood‐gatherer Anumbius annumbi?

Costs imposed by brood parasitic birds exert strong selection on their hosts to avoid parasitism. While egg rejection is a common defence, nestling rejection is rarer and less well understood. Theoretical models suggest that among non‐evicting parasites such as cowbirds nestling rejection can only evolve when levels of parasitism are high. Here we describe a possible case of early rejection of cowbird nestlings, by an infrequently parasitised host, the firewood‐gatherer Anumbius annumbi. Firewood‐gatherers accepted most shiny cowbird Molothrus bonariensis eggs despite clear differences in coloration. Cowbird eggs usually hatched 4–5 d before host eggs. All parasitic nestlings died within 48 h, and hosts continued their breeding attempts. Nestling death was most likely due to neglect since little food was found in the stomach of dead nestlings. Feeding neglect could be due to differences in visual or acoustic appearance between host and parasite hatchlings. Alternatively, hosts may refrain from feeding nestlings that hatch too early compared to their normal incubation time. At the moment our data do not allow distinction between active nestling recognition or cowbird nestling failure due to the unsuitability of the firewood‐gatherer as a host (i.e. too long incubation). Experiments are needed to tease these alternatives apart.     

Ontogenetic patterns of constitutive immune parameters in altricial house sparrows

Innate immune functions are proposed to develop rapidly post‐hatch in altricial nestlings, compared with adaptive immune defenses that require development of receptor specificity and memory. Studies of ontogenetic changes in altricial birds have been few until relatively recently and often do not encompass the entire developmental period. We examined the patterns of development in constitutive innate and adaptive immune indices in house sparrow nestlings (3, 6, 9 and 12 days (d) post‐hatch), hatch‐year birds and adults. Lysozyme activity significantly decreased with age, likely representing catabolism of maternal investment of lysozyme in the egg albumen. Levels of total IgY (indexing adaptive immune function), as well as agglutination and lysis (indexing innate immune function), increased throughout the nestling period, but were significantly below levels found in fully‐grown birds at the time of fledging. There were no significant differences between hatch‐year birds and adults in these measures, indicating that rapid, full maturation occurs early in the post‐fledging period. In combination with previous studies, these data highlight the importance of sampling fledglings to assess full immune ontogeny and suggest that fledgling birds may be more vulnerable to infection than adults.     

Origin-related, environmental, sex, and age determinants of immunocompetence, susceptibility to ectoparasites, and disease symptoms in the barn owl

Knowledge of the role of origin‐related, environmental, sex, and age factors on host defence mechanisms is important to understand variation in parasite intensity. Because alternative components of parasite defence may be differently sensitive to various factors, they may not necessarily covary. Many components should therefore be considered to tackle the evolution of host–parasite interactions. In a population of barn owls (Tyto alba), we investigated the role of origin‐related, environmental (i.e. year, season, nest of rearing, and body condition), sex, and age factors on 12 traits linked to immune responses [humoral immune responses towards sheep red blood cells (SRBC), human serum albumin (HSA) and toxoid toxin TT, T‐cell mediated immune response towards the mitogen phytohemagglutinin (PHA)], susceptibility to ectoparasites (number and fecundity of Carnus haemapterus, number of Ixodes ricinus), and disease symptoms (size of the bursa of Fabricius and spleen, proportion of proteins that are immunoglobulins, haematocrit and blood concentration in leucocytes). Cross‐fostering experiments allowed us to detect a heritable component of variation in only four out of nine immune and parasitic parameters (i.e. SRBC‐ and HSA‐responses, haematocrit, and number of C. haemapterus). However, because nestlings were not always cross‐fostered just after hatching, the finding that 44% of the immune and parasitic parameters were heritable is probably an overestimation. These experiments also showed that five out of these nine parameters were sensitive to the nest environment (i.e. SRBC‐ and PHA‐responses, number of C. haemapterus, haematocrit and blood concentration in leucocytes). Female nestlings were more infested by the blood‐sucking fly C. haemapterus than their male nestmates, and their blood was less concentrated in leucocytes. The effect of year, season, age (i.e. reflecting the degree of maturation of the immune system), brood size, position in the within‐brood age hierarchy, and body mass strongly differed between the 12 parameters. Different components of host defence mechanisms are therefore not equally heritable and sensitive to environmental, sex, and age factors, potentially explaining why most of these components did not covary. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90 , 703–718.     

Avoidance,tolerance, and resistance to ectoparasites in nestling and adult tree swallows

We examined avoidance, tolerance, and resistance strategies of nestling and adult tree swallows Tachycineta bicolor in response to ectoparasitic blowflies Protocalliphora sialia. Tree swallows avoided settling in north‐facing nest boxes early in the breeding season. These boxes were more likely to be parasitized later in the season, suggesting that box selection may facilitate blowfly avoidance. After experimentally manipulating blowfly intensity, we found that nestlings were generally tolerant of parasitism. Parasites significantly reduced nestling blood hemoglobin but had no effect on nestling body mass, primary feather growth, age at fledging, or fledging success. Parents of parasitized nestlings did not increase their food provisioning rate to promote nestling tolerance. Adult female tree swallows demonstrated both tolerance and resistance: blowfly parasitism had no effect on adult hemoglobin and body mass, and those with higher P. sialia‐binding antibody levels had fewer blowfly larvae in their nests. Nestling antibodies were unrelated to blowfly intensity. Despite considerable variation among years, our results suggest that the costs of blowfly parasitism to nestling and adult tree swallows are modest, and limited to blood loss in nestlings. Future work should examine the effects of reduced blood hemoglobin on fledgling survival and the importance of parasite‐specific antibodies.