Malarial parasites are supposed to have strong negative fitness consequences for their hosts, but relatively little evidence supports this claim due to the difficulty of experimentally testing this. We experimentally reduced levels of infection with the blood parasite Haemoproteus prognei in its host the house martin Delichon urbica, by randomly treating adults with primaquine or a control treatment. Treated birds had significantly fewer parasites than controls. The primaquine treatment increased clutch size by 18%; hatching was 39% higher and fledging 42% higher. There were no effects of treatment on quality of offspring, measured in terms of tarsus length, body mass, haematocrit or T-cell-mediated immune response. These findings demonstrate that malarial parasites can have dramatic effects on clutch size and other demographic variables, potentially influencing the evolution of clutch size, but also the population dynamics of heavily infected populations of birds.
Avian malaria parasites are supposed to exert negative effects on host fitness because these intracellular parasites affect host metabolism. Recent advances in molecular genotyping and microscopy have revealed that coinfections with multiple parasites are frequent in bird–malaria parasite systems. However, studies of the fitness consequences of such double infections are scarce and inconclusive. We tested if the infection with two malaria parasite lineages has more negative effects than single infection using 6 years of data from a natural population of house martins. Survival was negatively affected by both types of infections. We found an additive cost from single to double infection in body condition, but not in reproductive parameters (double‐infected had higher reproductive success). These results demonstrate that malaria infections decrease survival, but also have different consequences on the breeding performance of single‐ and double‐infected wild birds.
Invasive species can displace natives, and thus identifying the traits that make aliens successful is crucial for predicting and preventing biodiversity loss. Pathogens may play an important role in the invasive process, facilitating colonization of their hosts in new continents and islands. According to the Novel Weapon Hypothesis, colonizers may out-compete local native species by bringing with them novel pathogens to which native species are not adapted. In contrast, the Enemy Release Hypothesis suggests that flourishing colonizers are successful because they have left their pathogens behind. To assess the role of avian malaria and related haemosporidian parasites in the global spread of a common invasive bird, we examined the prevalence and genetic diversity of haemosporidian parasites (order Haemosporida, genera Plasmodium and Haemoproteus) infecting house sparrows (Passer domesticus). We sampled house sparrows (N = 1820) from 58 locations on 6 continents. All the samples were tested using PCR-based methods; blood films from the PCR-positive birds were examined microscopically to identify parasite species. The results show that haemosporidian parasites in the house sparrows' native range are replaced by species from local host-generalist parasite fauna in the alien environments of North and South America. Furthermore, sparrows in colonized regions displayed a lower diversity and prevalence of parasite infections. Because the house sparrow lost its native parasites when colonizing the American continents, the release from these natural enemies may have facilitated its invasion in the last two centuries. Our findings therefore reject the Novel Weapon Hypothesis and are concordant with the Enemy Release Hypothesis.
The social and ecological conditions that individuals experience during early development have marked effects on their developmental trajectory. In songbirds, brood size is a key environmental factor affecting development, and experimental increases in brood size have been shown to have negative effects on growth, condition and fitness. Possible causes of decreased growth in chicks from enlarged broods are nutritional stress, crowding and increased social competition, i.e. environmental factors known to affect adult steroid levels (especially of testosterone and corticosteroids) in mammals and birds. Little, however, is known about environmental effects on steroid synthesis in nestlings. We addressed this question by following the development of zebra finch (Taeniopygia guttata) chicks that were cross-fostered and raised in different brood sizes. In line with previous findings, nestling growth and cell-mediated immunocompetence were negatively affected by brood size. Moreover, nestling testosterone levels covaried with treatment: plasma testosterone increased with experimental brood size. This result provides experimental evidence that levels of circulating testosterone in nestlings can be influenced by their physiological response to environmental conditions.
The T‐cell mediated response to a challenge of the immune system with phytohemagglutinin (PHA) is a common measure used in ecological studies of host‐parasite interactions or parasite‐mediated selection. We investigated the temporal dynamics of this response in house sparrows Passer domesticus in order to determine factors that contribute to temporal and individual variation in PHA response. After an initial significant increase in response from injection to six hours post‐injection, there was no further significant change in mean response after 12, 24, 36, 48 and 72 hours. Responses at night were consistently stronger than during daytime. Individuals may benefit from producing both a strong and a quick immune response to parasite attacks, although this may be impossible because of the observed positive relationship between maximum response and latency to maximum response. House sparrows with Haemoproteus infections had lower PHA responses and smaller maximum responses than individuals without infections. Individuals in prime body condition had stronger PHA responses than individuals in poor condition. House sparrows with large diurnal fluctuations in body mass had a weaker maximum response than individuals with small fluctuations. Since individuals with Haemoproteus infections have large fluctuations in body mass, this result suggests that infected individuals with large fluctuations in mass are unable to mount a strong immune response.
Knowing the genetic variation that occurs in pathogen populations and how it is distributed across geographical areas is essential to understand parasite epidemiology, local patterns of virulence, and evolution of host‐resistance. In addition, it is important to identify populations of pathogens that are evolutionarily independent and thus ‘free’ to adapt to hosts and environments. Here, we investigated genetic variation in the globally distributed, highly invasive avian malaria parasite Plasmodium relictum, which has several distinctive mitochondrial haplotyps (cyt b lineages, SGS1, GRW11 and GRW4). The phylogeography of P. relictum was accessed using the highly variable nuclear gene merozoite surface protein 1 (MSP1), a gene linked to the invasion biology of the parasite. We show that the lineage GRW4 is evolutionarily independent of GRW11 and SGS1 whereas GRW11 and SGS1 share MSP1 alleles and thus suggesting the presence of two distinct species (GRW4 versus SGS1 and GRW11). Further, there were significant differences in the global distribution of MSP1 alleles with differences between GRW4 alleles in the New and the Old World. For SGS1, a lineage formerly believed to have both tropical and temperate transmission, there were clear differences in MSP1 alleles transmitted in tropical Africa compared to the temperate regions of Europe and Asia. Further, we highlight the occurrence of multiple MSP1 alleles in GRW4 isolates from the Hawaiian Islands, where the parasite has contributed to declines and extinctions of endemic forest birds since it was introduced. This study stresses the importance of multiple independent loci for understanding patterns of transmission and evolutionary independence across avian malaria parasites.
BackgroundIn a rapidly changing world, it is of fundamental importance to understand processes constraining or facilitating adaptation through microevolution. As different traits of an organism covary, genetic correlations are expected to affect evolutionary trajectories. However, only limited empirical data are available.Methodology/Principal FindingsWe investigate the extent to which multivariate constraints affect the rate of adaptation, focusing on four morphological traits often shown to harbour large amounts of genetic variance and considered to be subject to limited evolutionary constraints. Our data set includes unique long-term data for seven bird species and a total of 10 populations. We estimate population-specific matrices of genetic correlations and multivariate selection coefficients to predict evolutionary responses to selection. Using Bayesian methods that facilitate the propagation of errors in estimates, we compare (1) the rate of adaptation based on predicted response to selection when including genetic correlations with predictions from models where these genetic correlations were set to zero and (2) the multivariate evolvability in the direction of current selection to the average evolvability in random directions of the phenotypic space. We show that genetic correlations on average decrease the predicted rate of adaptation by 28%. Multivariate evolvability in the direction of current selection was systematically lower than average evolvability in random directions of space. These significant reductions in the rate of adaptation and reduced evolvability were due to a general nonalignment of selection and genetic variance, notably orthogonality of directional selection with the size axis along which most (60%) of the genetic variance is found.ConclusionsThese results suggest that genetic correlations can impose significant constraints on the evolution of avian morphology in wild populations. This could have important impacts on evolutionary dynamics and hence population persistence in the face of rapid environmental change.
Summary 1.We studied lifetime arrival patterns in the barn swallow (Hirundo rustica L.) in relation to variation in ecological conditions, as reflected by the normalized difference vegetation index (NDVI) in the Sub-Saharan winter quarters and at stopover sites in North Africa. 2. Migratory birds have recently advanced their arrival dates, but the relative role of microevolution and phenotypic plasticity as mechanisms of response to changing environmental conditions remains unknown. To distinguish between these two possibilities, we investigated the change in the arrival date using cross-sectional and longitudinal analyses. 3. We predicted that the effect (i.e. slopes) of environmental conditions in stopover or winter areas on arrival date should be similar using cross-sectional and longitudinal analyses in case phenotypic plasticity is the underlying mechanism, or they should differ in case microevolution is the mechanism. 4. As expected according to a previous cross-sectional study, we found an advance in the arrival date when ecological conditions improve in stopover areas and a delay in the arrival date when ecological conditions improve in the winter quarters. 5. Change in the arrival time at the breeding grounds due to ecological conditions found en route and, in the winter areas, was mainly due to phenotypic plasticity as shown by similarities in the slopes found in these relationships using cross-sectional and longitudinal analyses. 6. We also investigated sex and age of barns swallows as sources of variation in the arrival time with respect to conditions experienced in winter and stopover areas. We found that earlier arrival at the breeding grounds due to prevailing ecological conditions found en route in North Africa was similar for males and females of all age-classes. In contrast, individuals tended to delay departure when ecological conditions improved in the winter quarters, but this delay differed among age classes, with old individuals delaying departure more than middle-aged and yearling birds. 7. The migratory response of individuals to changing climatic conditions experienced during different parts of their life provides evidence for individuals responding differently to prevailing conditions in the winter quarters depending on their age, but not to conditions experienced en route during spring migration.
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