The experimental study on susceptibility of common European songbirds to Plasmodium elongatum (lineage pGRW6), a widespread avian malaria parasite.

BACKGROUND: Plasmodium elongatum (cytochrome b lineage pGRW6) is a widespread avian malaria parasite, often causing severe disease in non-adapted hosts. This parasite lineage is of global distribution however, its virulence remains insufficiently understood, particularly in wild birds. Surprisingly, this infection has never been reported in Common starlings Sturnus vulgaris and Common crossbills Loxia curvirostra, common European songbirds which were extensively sampled across Europe. A hypothesis was proposed that these birds might be resistant to the pGRW6 infection. The aim of this study was to test this hypothesis. METHODS: Lineage pGRW6 was isolated from a naturally infected Eurasian reed warbler, multiplied in vivo and inoculated in Common starlings and Common crossbills. Experimental and control groups (8 birds in each) were maintained in controlled conditions and examined microscopically every 4 days. Haematocrit value and body mass were monitored in parallel. At the end of the experiment (44 days post exposure), samples of internal organs were collected and examined using histological methods for possible presence of phanerozoites. RESULTS: All control birds remained uninfected. Experimental starlings were resistant. All exposed crossbills were susceptible and survived until the end of this study. Prepatent period was 12-16 days post exposure. Light parasitaemia (< 0.7%) developed in all birds, and only few phanerozoites were seen in bone marrow cells of 5 of 8 experimentally infected crossbills. Significant changes were reported only in haematocrit value but not body mass in the exposed crossbills compared to controls. CONCLUSION: Plasmodium elongatum (pGRW6) is of low virulence in Common crossbills and is unable to develop in Common starlings, indicating innate resistance of the later bird species. Low virulence in Common crossbills is likely due to the inability or low ability of this parasite lineage to develop phanerozoites resulting in light (if at all) damage of stem bone marrow cells. This study suggests that susceptibility of different bird species to the lineage pGRW6 is markedly variable. The global distribution of this parasite might be due to low virulence in wild adapted avian hosts, which survive this infection and serve as reservoirs host for non-adapted birds in whom this infection is often lethal.

GUT PARASITE LEVELS ARE ASSOCIATED WITH SEVERITY OF RESPONSE TO IMMUNE CHALLENGE IN A WILD SONGBIRD.

Life history trade-offs have been posited to shape wild animals' immune responses against microparasites (e.g., bacteria, viruses). However, coinfection with gut helminths may bias immune phenotypes away from inflammatory responses and could be another mechanism underlying variation in immune responses. We examined how the magnitude of a common and costly response to microparasites, the acute phase response (APR), varied with helminth coinfection at both the individual and the population levels in Song Sparrows ( Melospiza melodia). The APR includes fever and sickness behaviors, like lethargy and anorexia, and provides a whole-organism metric of immune activation. We combined data on fever and lethargy in response to an immune challenge (lipopolysaccharide) with postmortem data assessing helminth burdens and data on malarial parasite infection from blood samples in sparrows from two populations: southern California and western Washington, US. We predicted that birds with higher helminth burdens would express less severe APRs, at both the individual and population levels. Furthermore, we predicted that these reduced immune responses would diminish resistance against malarial parasites and would thus be associated with higher prevalences of such parasites. Previously, Song Sparrows from Washington have been shown to mount less severe APRs than those from California. In our study, Washington birds also exhibited higher helminth burdens and a higher prevalence of one type of avian malarial parasite. Because of low variation in helminth burdens in California (median=0, range=0-3), we tested within-population relationships only in birds from Washington, where the severity of fever and lethargy correlated negatively with helminth burden. These results suggested that helminth coinfection could help mediate immune responsiveness in wild songbirds.

Avian malaria and bird humoral immune response.

BACKGROUND: Plasmodium parasites are known to impose fitness costs on their vertebrate hosts. Some of these costs are due to the activation of the immune response, which may divert resources away from self-maintenance. Plasmodium parasites may also immuno-deplete their hosts. Thus, infected individuals may be less able to mount an immune response to a new pathogen than uninfected ones. However, this has been poorly investigated. METHODS: The effect of Plasmodium infection on bird humoral immune response when encountering a novel antigen was tested. A laboratory experiment was conducted on canaries (Serinus canaria) experimentally infected with Plasmodium relictum (lineage SGS1) under controlled conditions. Birds were immune challenged with an intra-pectoral injection of a novel non-pathogenic antigen (keyhole limpet haemocyanin, KLH). One week later they were challenged again. The immune responses to the primary and to the secondary contacts were quantified as anti-KLH antibody production via enzyme-linked immunosorbent assay (ELISA). RESULTS: There was no significant difference in antibody production between uninfected and Plasmodium infected birds at both primary and secondary contact. However, Plasmodium parasite intensity in the blood increased after the primary contact with the antigen. CONCLUSIONS: There was no effect of Plasmodium infection on the magnitude of the humoral immune response. However, there was a cost of mounting an immune response in infected individuals as parasitaemia increased after the immune challenge, suggesting a trade-off between current control of chronic Plasmodium infection and investment against a new immune challenge.

An experimental test of the physiological consequences of avian malaria infection.

Chronic, low-intensity parasite infections can reduce host fitness through negative impacts on reproduction and survival, even if they produce few overt symptoms. As a result, these parasites can influence the evolution of host morphology, behaviour and physiology. The physiological consequences of chronic infection can provide insight into the processes underlying parasite-driven natural selection. Here, we evaluate the physiological consequences of natural, low-intensity infection in an avian host-parasite system: adult male red-winged blackbirds (Agelaius phoeniceus) infected with haemosporidian parasites. Chronic haemosporidian infection has previously been shown to reduce both reproductive success and survival in several avian species. We used antimalarial medications to experimentally reduce haemosporidian parasitaemia (the proportion of blood cells infected with haemosporidian parasites) and measured the effect of treatment on body condition, haematology, immune function, physiological stress and oxidative state. Treatment with an antimalarial medication reduced parasitaemia for the most prevalent haemosporidian parasites from the genus Plasmodium. Treatment also increased haemoglobin and haematocrit, and decreased red blood cell production rates. We detected no effect of treatment on body condition, immune metrics, plasma corticosterone concentrations, total antioxidant capacity or reactive oxygen metabolites. Our results suggest that the damage and replacement of red blood cells during infection could be important costs of chronic haemosporidian infection. Strong links between parasitaemia and the physiological consequences of infection indicate that even for relatively low-intensity infections, measuring parasitaemia rather than only presence/absence could be important when evaluating the role of infection in influencing hosts' behaviour, physiology or fitness.

Host immune responses to experimental infection of Plasmodium relictum (lineage SGS1) in domestic canaries (Serinus canaria).

Understanding the complexity of host immune responses to parasite infection requires controlled experiments that can inform observational field studies. Birds and their malaria parasites provide a useful model for understanding host-parasite relationships, but this model lacks a well-described experimental context for how hosts respond immunologically to infection. Here, ten canaries (Serinus canaria) were infected with the avian malaria parasite Plasmodium relictum (lineage SGS1) in a controlled laboratory setting with ten uninfected (control) birds. A suite of immunological blood parameters, including the concentration of four white blood cell types, the concentration of the acute phase protein haptoglobin, and the bacteria-killing ability of blood plasma, were repeatedly measured over a 25-day period covering the acute phase of a primary infection by P. relictum. Three infected and one control bird died during the course of the experiment. A multivariate statistical analysis of the immune indices revealed significant differences between infected and uninfected individuals between 5 and 14 days postinfection (dpi). Group differences corresponded to reduced concentrations of lymphocytes (5 dpi), heterophils (8 dpi), and monocytes (11 and 14 dpi), and an increase in haptoglobin (14 dpi), in infected birds relative to uninfected controls, and no change in bacteria-killing. Upon re-running the analysis with only the surviving birds, immunological differences between infected and control birds shifted to between 11 and 18 dpi. However, there were no clear correlates relating immune parameters to the likelihood of surviving the infection. The results presented here demonstrate the dynamic and complex nature of avian immune function during the acute phase of malaria infection and provide a context for studies investigating immune function in wild birds.

Plasmodium spp.: an experimental study on vertebrate host susceptibility to avian malaria.

The interest in experimental studies on avian malaria caused by Plasmodium species has increased recently due to the need of direct information about host-parasite interactions. Numerous important issues (host susceptibility, development of infection, the resistance and tolerance to avian malaria) can be answered using experimental infections. However, specificity of genetically different lineages of malaria parasites and their isolates is largely unknown. This study reviews recent experimental studies and offers additional data about susceptibility of birds to several widespread cytochrome b (cyt b) lineages of Plasmodium species belonging to four subgenera. We exposed two domesticated avian hosts (canaries Serinus canaria and ducklings Anas platyrhynchos) and also 16 species of common wild European birds to malaria infections by intramuscular injection of infected blood and then tested them by microscopic examination and PCR-based methods. Our study confirms former field and experimental observations about low specificity and wide host-range of Plasmodium relictum (lineages SGS1 and GRW11) and P. circumflexum (lineage TURDUS1) belonging to the subgenera Haemamoeba and Giovannolaia, respectively. However, the specificity of different lineages and isolates of the same parasite lineage differed between species of exposed hosts. Several tested Novyella lineages were species specific, with a few cases of successful development in experimentally exposed birds. The majority of reported cases of mortality and high parasitaemia were observed during parasite co-infections. Canaries were susceptible mainly for the species of Haemamoeba and Giovannolaia, but were refractory to the majority of Novyella isolates. Ducklings were susceptible to three malaria infections (SGS1, TURDUS1 and COLL4), but parasitaemia was light (<0.01%) and transient in all exposed birds. This study provides novel information about susceptibility of avian hosts to a wide array of malaria parasite lineages, outlining directions for future experimental research on various aspects of biology and epidemiology of avian malaria.

How important are hemoparasites to migratory songbirds? Evaluating physiological measures and infection status in three neotropical migrants during stopover.

Long-distance migrations are energetically expensive for many animals, including migratory songbirds. During these demanding journeys, birds likely face limitations in allocating resources to different physiological functions, including lipid reserves needed to fuel the migration and costly immune defense against pathogens. We sampled three species of long-distance migratory songbirds during their fall migration through coastal Georgia and quantified their body condition, subcutaneous fat reserves, and infection status with blood parasites (Hemoproteus and Plasmodium). We also quantified cellular immunity, on the basis of total and differential white blood cell counts, and estimated individual stress levels, using the heterophil∶lymphocyte (H∶L) ratio. We tested whether birds infected with blood parasites had decreased fat measures, poorer body condition, or increased stress levels (as reflected by H∶L ratios). We also examined relationships between immune cell profiles and the following variables: body condition, subcutaneous fat, infection status, age, and species. Infected birds did not show greater H∶L ratios, poorer body condition, or lower fat measures, but in one species infected individuals showed significantly elevated leukocyte counts. Although we found little evidence for negative relationships between immune cell counts and body condition or fat measures, as might reflect underlying trade-offs in resource allocation, our results concerning hemoparasites are consistent with past work and suggest that chronic hemoparasite infections might have minimal effects on the outcome of long-distance migratory flight.

The ecology of host immune responses to chronic avian haemosporidian infection.

Host responses to parasitism in the wild are often studied in the context of single host-parasite systems, which provide little insight into the ecological dynamics of host-parasite interactions within a community. Here we characterized immune system responses to mostly low-intensity, chronic infection by haemosporidian parasites in a sample of 424 individuals of 22 avian host species from the same local assemblage in the Missouri Ozarks. Two types of white blood cells (heterophils and lymphocytes) were elevated in infected individuals across species, as was the acute-phase protein haptoglobin, which is associated with inflammatory immune responses. Linear discriminant analysis indicated that individuals infected by haemosporidians occupied a subset of the overall white blood cell multivariate space that was also occupied by uninfected individuals, suggesting that these latter individuals might have harbored other pathogens or that parasites more readily infect individuals with a specific white blood cell profile. DNA sequence-defined lineages of haemosporidian parasites were sparsely distributed across the assemblage of hosts. In one well-sampled host species, the red-eyed vireo (Vireo olivaceus), heterophils were significantly elevated in individuals infected with one but not another of two common parasite lineages. Another well-sampled host, the yellow-breasted chat (Icteria virens), exhibited no differences in immune response to different haemosporidian lineages. Our results indicate that while immune responses to infection may be generalized across host species, parasite-specific immune responses may also occur.

MHC-I affects infection intensity but not infection status with a frequent avian malaria parasite in blue tits.

Host resistance against parasites depends on three aspects: the ability to prevent, control and clear infections. In vertebrates the immune system consists of innate and adaptive immunity. Innate immunity is particularly important for preventing infection and eradicating established infections at an early stage while adaptive immunity is slow, but powerful, and essential for controlling infection intensities and eventually clearing infections. Major Histocompatibility Complex (MHC) molecules are central in adaptive immunity, and studies on parasite resistance and MHC in wild animals have found effects on both infection intensity (parasite load) and infection status (infected or not). It seems MHC can affect both the ability to control infection intensities and the ability to clear infections. However, these two aspects have rarely been considered simultaneously, and their relative importance in natural populations is therefore unclear. Here we investigate if MHC class I genotype affects infection intensity and infection status with a frequent avian malaria infection Haemoproteus majoris in a natural population of blue tits Cyanistes caeruleus. We found a significant negative association between a single MHC allele and infection intensity but no association with infection status. Blue tits that carry a specific MHC allele seem able to suppress H. majoris infection intensity, while we have no evidence that this allele also has an effect on clearance of the H. majoris infection, a result that is in contrast with some previous studies of MHC and avian malaria. A likely explanation could be that the clearance rate of avian malaria parasites differs between avian malaria lineages and/or between avian hosts.

Immunity, resistance and tolerance in bird-parasite interactions.

Interacting pathogens and hosts have evolved reciprocal adaptations whose function is to allow host exploitation (from the pathogen stand point) or minimize the cost of infection (from the host stand point). Once infected, two strategies are offered to the host: parasite clearing (resistance) and withstanding the infection while paying a low fitness cost (tolerance). In both cases, the immune system plays a central role. Interestingly, whatever the defence strategy adopted by the host, this is likely to have an effect on parasite evolution. Given their short generation time and large population size, parasites are expected to rapidly adapt to the environmental conditions provided by their hosts. The immune system can therefore represent a powerful engine of parasite evolution, with the direction of such evolutionary trajectory depending on, among other factors, (i) the type of mechanism involved (resistance or tolerance) and (ii) the damage induced by overreacting immune defences. In this article, I will discuss these different issues focusing on selected examples of recent work conducted on two bird pathogens, the protozoa responsible for avian malaria (Plasmodium sp.) and the bacterium Mycoplasma gallisepticum.

Experimental evidence for evolved tolerance to avian malaria in a wild population of low elevation Hawai'i 'Amakihi (Hemignathus virens).

Introduced vector-borne diseases, particularly avian malaria (Plasmodium relictum) and avian pox virus (Avipoxvirus spp.), continue to play significant roles in the decline and extinction of native forest birds in the Hawaiian Islands. Hawaiian honeycreepers are particularly susceptible to avian malaria and have survived into this century largely because of persistence of high elevation refugia on Kaua'i, Maui, and Hawai'i Islands, where transmission is limited by cool temperatures. The long term stability of these refugia is increasingly threatened by warming trends associated with global climate change. Since cost effective and practical methods of vector control in many of these remote, rugged areas are lacking, adaptation through processes of natural selection may be the best long-term hope for recovery of many of these species. We document emergence of tolerance rather than resistance to avian malaria in a recent, rapidly expanding low elevation population of Hawai'i 'Amakihi (Hemignathus virens) on the island of Hawai'i. Experimentally infected low elevation birds had lower mortality, lower reticulocyte counts during recovery from acute infection, lower weight loss, and no declines in food consumption relative to experimentally infected high elevation Hawai'i 'Amakihi in spite of similar intensities of infection. Emergence of this population provides an exceptional opportunity for determining physiological mechanisms and genetic markers associated with malaria tolerance that can be used to evaluate whether other, more threatened species have the capacity to adapt to this disease.

Experimental inhibition of nitric oxide increases Plasmodium relictum (lineage SGS1) parasitaemia.

Malaria is a widespread vector-borne disease infecting a wide range of terrestrial vertebrates including reptiles, birds and mammals. In addition to being one of the most deadly infectious diseases for humans, malaria is a threat to wildlife. The host immune system represents the main defence against malaria parasites. Identifying the immune effectors involved in malaria resistance has therefore become a major focus of research. However, this has mostly involved humans and animal models (rodents) and how the immune system regulates malaria progression in non-model organisms has been largely ignored. The aim of the present study was to investigate the role of nitric oxide (NO) as an immune effector contributing to the control of the acute phase of infection with the avian malaria agent Plasmodium relictum. We used experimental infections of domestic canaries in conjunction with the inhibition of the enzyme inducible nitric oxide synthase (iNOS) to assess the protective function of NO during the infection, and the physiological costs paid by the host in the absence of an effective NO response. Our results show that birds treated with the iNOS inhibitor suffered from a higher parasitaemia, but did not pay a higher cost of infection (anaemia). While these findings confirm that NO contributes to the resistance to avian malaria during the acute phase of the infection, they also suggest that parasitaemia and costs of infection can be decoupled.

MHC diversity, malaria and lifetime reproductive success in collared flycatchers.

Major histocompatibility complex (MHC) genes encode proteins involved in the recognition of parasite-derived antigens. Their extreme polymorphism is presumed to be driven by co-evolution with parasites. Host-parasite co-evolution was also hypothesized to optimize within-individual MHC diversity at the intermediate level. Here, we use unique data on lifetime reproductive success (LRS) of female collared flycatchers to test whether LRS is associated with within-individual MHC class II diversity. We also examined the association between MHC and infection with avian malaria. Using 454 sequencing, we found that individual flycatchers carry between 3 and 23 functional MHC class II B alleles. Predictions of the optimality hypothesis were not confirmed by our data as the prevalence of blood parasites decreased with functional MHC diversity. Furthermore, we did not find evidence for an association between MHC diversity and LRS.

Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress.

Parental effort is usually associated with high metabolism that could lead to an increase in the production of reactive oxidative species giving rise to oxidative stress. Since many antioxidants involved in the resistance to oxidative stress can also enhance immune function, an increase in parental effort may diminish the level of antioxidants otherwise involved in parasite resistance. In the present study, we performed brood size manipulation in a population of great tits (Parus major) to create different levels of parental effort. We measured resistance to oxidative stress and used a newly developed quantitative PCR assay to quantify malarial parasitaemia. We found that males with an enlarged brood had significantly higher level of malarial parasites and lower red blood cell resistance to free radicals than males rearing control and reduced broods. Brood size manipulation did not affect female parasitaemia, although females with an enlarged brood had lower red blood cell resistance than females with control and reduced broods. However, for both sexes, there was no relationship between the level of parasitaemia and resistance to oxidative stress, suggesting a twofold cost of reproduction. Our results thus suggest the presence of two proximate and independent mechanisms for the well-documented trade-off between current reproductive effort and parental survival.

Plasmodium relictum infection and MHC diversity in the house sparrow (Passer domesticus).

Antagonistic coevolution between hosts and parasites has been proposed as a mechanism maintaining genetic diversity in both host and parasite populations. In particular, the high level of genetic diversity usually observed at the major histocompatibility complex (MHC) is generally thought to be maintained by parasite-driven selection. Among the possible ways through which parasites can maintain MHC diversity, diversifying selection has received relatively less attention. This hypothesis is based on the idea that parasites exert spatially variable selection pressures because of heterogeneity in parasite genetic structure, abundance or virulence. Variable selection pressures should select for different host allelic lineages resulting in population-specific associations between MHC alleles and risk of infection. In this study, we took advantage of a large survey of avian malaria in 13 populations of the house sparrow (Passer domesticus) to test this hypothesis. We found that (i) several MHC alleles were either associated with increased or decreased risk to be infected with Plasmodium relictum, (ii) the effects were population specific, and (iii) some alleles had antagonistic effects across populations. Overall, these results support the hypothesis that diversifying selection in space can maintain MHC variation and suggest a pattern of local adaptation where MHC alleles are selected at the local host population level.

Pathogenic action of Plasmodium gallinaceum in chickens: brain histology and nitric oxide production by blood monocyte-derived macrophages.

Plasmodium infection causes major losses to animal and human populations. The characterization of experimental malaria models is needed for a better understanding of disease mechanisms and the development of new treatment protocols. Chickens infected with Plasmodium gallinaceum constitute an adequate malaria model due to the phylogenetic proximity of this parasite to human Plasmodium as well as similarities in disease manifestation, such as cerebral malaria. The aim of the present study was to further characterize the experimental chicken model with an emphasis on clinical manifestations, cerebral histology and nitric oxide (NO) produced by macrophages. The results revealed that mortality was correlated to higher parasitemia. Parasitemia was positively correlated to temperature and negatively correlated to haematocrit value. Brain histology of infected birds revealed inflammatory infiltrates and blocked microvasculature. Macrophages derived from blood monocytes produced NO after activation, with a higher production positively correlated to parasitemia. These results characterize histological aspects of chicken brain malaria and demonstrate the activation of the innate immune system caused by the infection in chickens.

Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds.

We evaluated the effects of Plasmodium relictum (lineage P-SGS1), which is a host generalist, to five species of passerine birds. Light infection of P. relictum was isolated from a naturally infected adult reed warbler Acrocephalus scirpaceus. The parasites were inoculated to naive juveniles of the chaffinch Fringilla coelebs, common crossbill Loxia curvirostra, house sparrow Passer domesticus, siskin Spinus spinus and starling Sturnus vulgaris. Susceptibility of these birds to the infection of P. relictum was markedly different. This parasite developed in birds belonging to the Fringillidae and Passeridae but the starlings (Sturnidae) were resistant. Only 50% of experimental house sparrows were susceptible to the infection. The intensity of parasitemia varied markedly inside and between different susceptible bird species. There were no effects of the infection on body mass or temperature of experimentally infected birds. Infection of P. relictum leads to the significant decrease of haematocrit value and hypertrophy of spleen and liver in heavily infected common crossbills and siskins. This study shows that infection of the same lineage of P. relictum causes diseases of different severity in different avian hosts; that might have different evolutionary consequences and should be taken in consideration in conservation projects.

Exoerythrocytic development of Plasmodium gallinaceum in the White Leghorn chicken.

Plasmodium gallinaceum typically causes sub-clinical disease with low mortality in its primary host, the Indian jungle fowl Gallus sonnerati. Domestic chickens of European origin, however, are highly susceptible to this avian malaria parasite. Here we describe the development of P. gallinaceum in young White Leghorn chicks with emphasis on the primary exoerythrocytic phase of the infection. Using various regimens for infection, we found that P. gallinaceum induced a transient primary exoerythrocytic infection followed by a fulminant lethal erythrocytic phase. Prerequisite for the appearance of secondary exoerythrocytic stages was the development of a certain level of parasitaemia. Once established, secondary exoerythrocytic stages could be propagated from bird to bird for several generations without causing fatalities. Infected brains contained large secondary exoerythrocytic stages in capillary endothelia, while in the liver primary and secondary erythrocytic stages developed primarily in Kupffer cells and remained smaller. At later stages, livers exhibited focal hepatocyte necrosis, Kupffer cell hyperplasia, stellate cell proliferation, inflammatory cell infiltration and granuloma formation. Because P. gallinaceum selectively infected Kupffer cells in the liver and caused a histopathology strikingly similar to mammalian species, this avian Plasmodium species represents an evolutionarily closely related model for studies on the hepatic phase of mammalian malaria.

No relationship between individual genetic diversity and prevalence of avian malaria in a migratory kestrel.

Insight into the genetic basis of malaria resistance is crucial for understanding the consequences of this parasite group on animal populations. Here, we analyse the relationship between genotypic variation at 11 highly variable microsatellite loci and prevalence of three different lineages of avian malaria, two Plasmodium (RTSR1, LK6) and one Haemoproteus (LK2), in a wild population of the endangered lesser kestrel (Falco naumanni). Although we used a large sample size (584 typed individuals), we did not find any significant association between the prevalence of the studied parasite lineages and individual genetic diversity. Although our data set is large, the 11 neutral markers typed may have had low power to detect such association, in part because of the low parasite prevalence observed (less than 5% of infected birds). However, the fact that we have detected previous correlations between genetic diversity and other traits (ectoparasitism risk, fecundity) in the study population using the same panel of neutral markers and lower sample sizes suggests that other factors could underlie the absence of such a similar correlation with avian malaria. Differences in the genetics of the studied traits and in their particular basis of inbreeding depression (dominance vs. overdominance) may have led to malaria prevalence, but not other traits, being uncoupled with individual genetic diversity. Also, we cannot discard the possibility that the absence of association was a consequence of a low pathogenic effect of these particular malaria lineages on our lesser kestrel population, and thus we should not expect the evolution of genetic resistance against these parasites.

Contrasting adaptive immune defenses and blood parasite prevalence in closely related Passer sparrows.

Immune system components differ in their functions and costs, and immune defense profiles are likely to vary among species with differing ecologies. We compared adaptive immune defenses in two closely related species that have contrasting inflammatory immune responses, the widespread and abundant house sparrow (Passer domesticus) and the less abundant tree sparrow (Passer montanus). We found that the house sparrow, which we have previously shown mounts weaker inflammatory responses, exhibits stronger adaptive immune defenses, including antibody responses, natural antibody titers, and specific T-cell memory, than the tree sparrow. Conversely, tree sparrows, which mount strong inflammatory responses, also mount stronger nonspecific inflammatory T-cell responses but weaker specific adaptive responses. Prevalence of avian malaria parasite infections, which are controlled by adaptive immune defenses, was higher in the geographically restricted tree sparrow than in the ubiquitous house sparrow. Together these data describe distinct immune defense profiles between two closely related species that differ greatly in numbers and distributions. We suggest that these immunological differences could affect fitness in ways that contribute to the contrasting abundances of the two species in North American and Western Europe.