Within-population variation in prevalence and lineage distribution of avian malaria in blue tits, Cyanistes caeruleus

The development of molecular genetic screening techniques for avian blood parasites has revealed many novel aspects of their ecology, including greatly elevated diversity and complex host-parasite relationships. Many previous studies of malaria in birds have treated single study populations as spatially homogeneous with respect to the likelihood of transmission of malaria to hosts, and we have very little idea whether any spatial heterogeneity influences different malaria lineages similarly. Here, we report an analysis of variation in the prevalence and cytochrome b lineage distribution of avian malaria infection with respect to environmental and host factors, and their interactions, in a single blue tit (Cyanistes caeruleus) population. Of 11 Plasmodium and Haemoproteus cytochrome b lineages found in 997 breeding individuals, the three most numerous (pSGS1, pTURDUS1 and pBT7) were considered separately, in addition to analyses of all avian malaria lineages pooled. Our analyses revealed marked spatial differences in the prevalence and distribution of these lineages, with local prevalence of malaria within the population ranging from over 60% to less than 10%. In addition, we found several more complex patterns of prevalence with respect to local landscape features, host state, parasite genotype, and their interactions. We discuss the implications of such heterogeneity in parasite infection at a local scale for the study of the ecology and evolution of infectious diseases in natural populations. The increased resolution afforded by the combination of molecular genetic and geographical information systems (GIS) tools has the potential to provide many insights into the epidemiology, evolution and ecology of these parasites in the future.     

Corticosterone metabolites in blue tit and pied flycatcher droppings: effects of brood size, ectoparasites and temperature

The hypothalamic-pituitary-adrenal (HPA) axis of birds induces the secretion of corticosterone (CORT) as a response to different ecological variables. In this study we tested experimentally if manipulations of brood size or ectoparasitism led to subsequent differences in the concentration of excreted CORT metabolites of adult and nestling blue tits (Cyanistes caeruleus). No significant effect of the manipulation of brood size was detected in adults or nestlings. No significant effect of ectoparasitism was detected in males or nestlings, although females from uninfested nests showed lower concentrations of excreted CORT metabolites. In addition, we analysed if weather conditions had an influence on the concentration of excreted CORT metabolites of blue tits and pied flycatchers (Ficedula hypoleuca) breeding in the same forest. We detected no effect of weather conditions on adults, but nestlings of both species showed a negative correlation between their excreted CORT metabolites and the average mean temperatures they were subjected to during their growth. This effect was not found in blue tits in a colder year, suggesting that the sensitivity of the HPA axis to ambient temperature may be subjected to interannual variation. Moreover, we found a positive effect of the maximum temperature on the day of sampling on the concentration of CORT metabolites of blue tit nestlings in one of the years. These results suggest that weather conditions may act as environmental stressors to which the HPA axis of blue tit and pied flycatcher nestlings may be sensitive.     

Diversity and host assemblage of avian haemosporidians in different terrestrial ecoregions of Peru

Characterizing the diversity and structure of host–parasite communities is crucial to understanding their eco-evolutionary dynamics. Malaria and related haemosporidian parasites are responsible for fitness loss and mortality in bird species worldwide. However, despite exhibiting the greatest ornithological biodiversity, avian haemosporidians from Neotropical regions are quite unexplored. Here, we analyze the genetic diversity of bird haemosporidian parasites (Plasmodium and Haemoproteus) in 1,336 individuals belonging to 206 bird species to explore for differences in diversity of parasite lineages and bird species across 5 well-differentiated Peruvian ecoregions. We detected 70 different haemosporidian lineages infecting 74 bird species. We showed that 25 out of the 70 haplotypes had not been previously recorded. Moreover, we also identified 81 new host–parasite interactions representing new host records for these haemosporidian parasites. Our outcomes revealed that the effective diversity (as well as the richness, abundance, and Shannon–Weaver index) for both birds and parasite lineages was higher in Amazon basin ecoregions. Furthermore, we also showed that ecoregions with greater diversity of bird species also had high parasite richness, hence suggesting that host community is crucial in explaining parasite richness. Generalist parasites were found in ecoregions with lower bird diversity, implying that the abundance and richness of hosts may shape the exploitation strategy followed by haemosporidian parasites. These outcomes reveal that Neotropical region is a major reservoir of unidentified haemosporidian lineages. Further studies analyzing host distribution and specificity of these parasites in the tropics will provide important knowledge about phylogenetic relationships, phylogeography, and patterns of evolution and distribution of haemosporidian parasites.     

MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages

Research in avian blood parasites has seen a remarkable increase since the introduction of polymerase chain reaction-based methods for parasite identification. New data are revealing complex multihost-multiparasite systems which are difficult to understand without good knowledge of the host range and geographical distribution of the parasite lineages. However, such information is currently difficult to obtain from the literature, or from general repositories such as GenBank, mainly because (i) different research groups use different parasite lineage names, (ii) GenBank entries frequently refer only to the first host and locality at which each parasite was sampled, and (iii) different researchers use different gene fragments to identify parasite lineages. We propose a unified database of avian blood parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon identified by a partial region of their cytochrome b sequences. The database uses a standardized nomenclature to remove synonymy, and concentrates all available information about each parasite in a public reference site, thereby facilitating access to all researchers. Initial data include a list of host species and localities, as well as genetic markers that can be used for phylogenetical analyses. The database is free to download and will be regularly updated by the authors. Prior to publication of new lineages, we encourage researchers to assign names to match the existing database. We anticipate that the value of the database as a source for determining host range and geographical distribution of the parasites will grow with its size and substantially enhance the understanding of this remarkably diverse group of parasites.     

On the specificity of avian blood parasites: revealing specific and generalist relationships between haemosporidians and biting midges

The study of host-parasite relationships involving vector-borne parasites requires understanding interactions between parasites and vectors. The capacity of haemosporidians to infect insects has clear evolutionary consequences for the transmission of diseases. Here, we investigated (i) the associations between blood parasites, biting midges and birds and (ii) the potential specificity between biting midge and haemosporidian haplotypes. A total of 629 parous biting midges Culicoides and 224 wild birds (belonging to seven species) from a locality of central Spain were individually examined for the presence of Haemoproteus and Plasmodium parasites by sequencing a fragment of cytochrome B. Biting midges were identified morphologically and characterized on the basis of a fragment of the cytochrome c oxidase (COI) gene. Overall, 12 Haemoproteus and three Plasmodium haplotypes were isolated and sequenced. Among them, 10 haplotypes were exclusively isolated from biting midges, three haplotypes only from birds and two haplotypes from both biting midges and birds. Biting midge haplotypes showed both specific and generalist relationships with Haemoproteus haplotypes but only generalist relationships with Plasmodium haplotypes. Several C. festivipennis and C. kibunesis haplotypes established significant coevolutionary links with Haemoproteus haplotypes. These results shed light on the specificity of interactions between vectors and blood parasites.     

Ticks (Acari: Ixodoidea) in China: Geographical distribution,host diversity,and specificity

Ticks are obligate blood‐sucking ectoparasites, which not only directly damage through bites but also transmit many pathogens. China has a high diversity of tick species, 125 species have been reported, including 111 hard tick and 14 soft tick species. Many of the ticks are important vectors of pathogens, resulting in zoonoses. The dynamics of ticks are affected by both the host and habitat environment. However, systematic studies on the geographical distribution, host diversity, and specificity of ticks are limited in China. To achieve this goal, the relevant available data were summarized and analyzed in this study. Ticks are distributed in all parts of China and Xinjiang has the most records of ticks. The distribution of ticks in adjacent areas is similar, indicating that the habitat environment affects their distribution. Most ticks are widely distributed, whereas some species are endemic to their distributed regions. Ticks are parasitic on mammals, birds, and reptiles, of which mammals are the main host species. Overall, most ticks parasitize different hosts, only a few ticks have strict host specificity, such as ticks that are specifically parasitic on reptiles and bats. In addition, environmental changes and control efforts also influence the dynamics of ticks. These results can better reveal tick biological traits and are valuable for tick control.     

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.     

Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles

We identify and describe the distribution of 12 genetically distinct malaria parasite lineages over islands and hosts in four common passerine birds in the Lesser Antilles. Combined parasite prevalence demonstrates strong host effects, little or no island effect, and a significant host-times-island interaction, indicating independent outcomes of host-parasite infections among island populations of the same host species. Host- and/or island-specific parasite lineages do not explain these host-parasite associations; rather, individual lineages themselves demonstrate the same type of independent interactions. Unlike overall prevalence, individual parasite lineages show considerable geographic structure (i.e., island effects) as well as species effects indicating that parasite lineages are constrained in their ability to move between hosts and locations. Together, our results suggest an upper limit to the number of host individuals that malaria parasites, as a community, can infect. Within this limit, however, the relative frequency of the different lineages varies reflecting fine scale interactions between host and parasite populations. Patterns of host-parasite associations within this system suggest both historical co-evolution and ecologically dynamic and independent host-parasite interactions.     

Feathers,suspicions, and infidelities: an experimental study on parental care and certainty of paternity in the blue tit

Theoretical models on parental care predict that males should decrease their parental effort when paternity is in doubt. Males may use some cues to assess their certainty of paternity, and try to avoid rearing offspring sired by extra‐pair males. We have previously reported in a socially monogamous passerine, the blue tit (Cyanistes caeruleus), that males decorate their nests with feathers, and that when this ornament is manipulated, males appear to have suspicions about the presence of an intruder male. Here, we decrease the male's certainty of paternity through experimental feather supplementation to analyse whether the outcome of our experiment supports the assumptions of the parental care theory. Male C. caeruleus responded to the feather supplementation experiment by reducing their parental investment (feeding frequency and nest defence) in comparison with control males. The occurrence of extra‐pair offspring in experimental nests was double than that in controls. This suggests that the manipulation was successful not only in altering males' perceived paternity, but also, indirectly, the actual paternity. Furthermore, males that gained extra‐pair young also had a higher than average probability to lose paternity in their nest, which may imply that male C. caeruleus faced a trade‐off between obtaining extra‐pair fertilizations and maintaining paternity in their own nest. Overall, this study supports the idea that males are prone to decrease their parental effort when they perceive that the risk of losing paternity is high. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 552–561.     

Diversification by host switching and dispersal shaped the diversity and distribution of avian malaria parasites in Amazonia

Understanding how pathogens and parasites diversify through time and space is fundamental to predicting emerging infectious diseases. Here, we use biogeographic, coevolutionary and phylogenetic analyses to describe the origin, diversity, and distribution of avian malaria parasites in the most diverse avifauna on Earth. We first performed phylogenetic analyses using the mitochondrial cytochrome b (cyt b) gene to determine relationships among parasite lineages. Then, we estimated divergence times and reconstructed ancestral areas to uncover how landscape evolution has shaped the diversification of Parahaemoproteus and Plasmodium in Amazonia. Finally, we assessed the coevolutionary patterns of diversification in this host–parasite system to determine how coevolution may have influenced the contemporary diversity of avian malaria parasites and their distribution among Amazonian birds. Biogeographic analysis of 324 haemosporidian parasite lineages recovered from 4178 individual birds provided strong evidence that these parasites readily disperse across major Amazonian rivers and this has occurred with increasing frequency over the last five million years. We also recovered many duplication events within areas of endemism in Amazonia. Cophylogenetic analyses of these blood parasites and their avian hosts support a diversification history dominated by host switching. The ability of avian malaria parasites to disperse geographically and shift among avian hosts has played a major role in their radiation and has shaped the current distribution and diversity of these parasites across Amazonia.     

Prevalence and intensity of avian malaria in a quail hybrid zone

Hybrid zones have been described as natural laboratories by researchers who study speciation and the various mechanisms that may affect gene flow. The evolutionary consequences of hybridization depend not only on reproductive compatibility between sympatric species, but also on factors like vulnerability to each other''s predators and parasites. We examined infection patterns of the blood parasite Haemoproteus lophortyx, a causative agent of avian malaria, at a site in the contact zone between California quail (Callipepla californica) and Gambel''s quail (C. gambelii). Controlling for the potential influence of sex and year, we tested whether species identity predicted infection status and intensity. We found that infection prevalence was lower in California and hybrid quail compared with Gambel''s quail. However, infected California and hybrid quail had higher infection intensities than Gambel''s quail. California and hybrid quail exhibited no significant differences in prevalence or intensity of infection. These findings suggest that infection by H. lophortyx has the potential to influence species barrier dynamics in this system; however, more work is necessary to determine the exact evolutionary consequences of this blood parasite on hybridization.     

Temporal dynamics and diversity of avian malaria parasites in a single host species

1. We have used molecular methods to unravel a remarkable diversity of parasite lineages in a long-term population study of great reed warblers Acrocephalus arundinaceus that was not foreseen from traditional microscopic examination of blood smears. This diversity includes eight Haemoproteus and 10 Plasmodium lineages of which most probably represent good biological species. 2. Contrary to expectation, the relative frequency of parasite lineages seemed not to change over the 17-year study period and we found no effects of the parasites on a male secondary sexual ornament (song repertoire size) and two measures of fitness (adult survival and production of recruited offspring). 3. We discuss whether the absence of fitness consequences of the parasites might relate to the fact that we have studied the host at the breeding sites in Europe, whereas the transmission seems to take place at the wintering sites in Africa, where the na?ve birds encounter the parasites for the first time and the resulting primary infections likely make them sicker than during the chronic phase of the infection. 4. The prevalence of the three most common lineages appeared to fluctuate in parallel with a periodicity of approximately 3-4 years. Theoretical models based on intrinsic interactions between parasite antigen and host immune genes cannot explain such dynamics, suggesting that knowledge of extrinsic parameters such as vector distribution and alternative hosts are required to understand these patterns.     

Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda)

Organisms with wide geographical or phenotypic diversity often constitute assemblages of genetically distinct species or lineages. Within parasites, an emergence of host-specific lineages is assumed to create such cryptic variability; however, empirical evaluation of these processes is scarce. Here, we analyse populations of a parasite with a complex life cycle, wide host spectrum and global distribution, with the aim to reveal factors underlying the evolution of host- or geography-dependent lineages. Using 15 microsatellite loci, deep genetic distances were observed between populations from distant geographical areas. On the local scale, host-mediated genetic structure was found among sympatric samples. Two lineages differing in the spectrum of infected hosts co-occurred in the Euro-Mediterranean area, and two distinct lineages were recovered from Lake Tana in Ethiopia. Although sampled across several host taxa and multiple localities, a lack of marked genetic structure was seen in the populations belonging to one of the European lineages. Only weak genetic differentiation between sympatric samples from two host species was found. Complexity of the parasite life-cycle contributed to such a stratified pattern. Differences in the immune response between fish hosts were suggested as the factor diversifying the populations locally; conversely, high mobility of the parasite due to migration with its bird (definitive) host were assessed to homogenize populations across the area of distribution. However, despite the high mobility, large bodies of salt water prevent the parasite from long-distance migrations, as was demonstrated in an example of the Mediterranean Sea which represented an effective barrier to gene flow.     

Haematozoa in forest birds from southern Chile: Latitudinal gradients in prevalence and parasite lineage richness

Abstract The existence of latitudinal gradients in species richness and their abundance is known for many free living organisms but few cases have been reported for parasitic diseases. In addition, asymmetries between the Northern and Southern Hemispheres in several characteristics may affect the distribution and diversity of species at all ecological levels. In this respect, we study the distribution of several genera of blood parasites infecting birds along a latitudinal gradient that includes the world's southernmost forests ecosystems. Birds were mist‐netted and sampled for blood in localities across Chile ranging from 33°S to 55°S during the years 2003–06. Overall, 26 bird species were sampled and 27 parasite lineages were identified. The latter belonged to three genera: Plasmodium (8), Haemoproteus (8) and Leucocytozoon (11). We found a positive significant relationship between prevalence and latitude for Leucocytozoon lineages and a negative relationship for Haemoproteus, Plasmodium and mixed infections. However, we did not find a significant relationship between parasite diversity and latitude. We found 18 lineages infecting only one species of host, and 19 lineages appear in only one of the localities of sampling. This pattern implies that some parasite lineages may evolve in isolation in some species/localities. In addition, specificity at the host‐family level was only found for Haemoproteus lineages infecting birds in the family Emberizidae. Individuals of the long distance migrant bird white‐crested elaenia (Elaenia albiceps), were found infected by the same parasite lineages in localities separated by 20° of latitude. Infections by these lineages were detected in other sedentary birds including juveniles and nestlings of different bird species. Therefore, long distance migrants are able to distort the presence of latitudinal gradients of diseases due to the potential role of migrants in spreading infections. Geographical gradients in prevalence of avian haematozoa differ between parasite genera and hemispheres, probably in relation to the existence of appropriate vector–parasite–host interactions.     

Contrasting the seasonal and elevational prevalence of generalist avian haemosporidia in co‐occurring host species

Understanding the ecology and evolution of parasites is contingent on identifying the selection pressures they face across their infection landscape. Such a task is made challenging by the fact that these pressures will likely vary across time and space, as a result of seasonal and geographical differences in host susceptibility or transmission opportunities. Avian haemosporidian blood parasites are capable of infecting multiple co‐occurring hosts within their ranges, yet whether their distribution across time and space varies similarly in their different host species remains unclear. Here, we applied a new PCR method to detect avian haemosporidia (genera Haemoproteus, Leucocytozoon, and Plasmodium) and to determine parasite prevalence in two closely related and co‐occurring host species, blue tits (Cyanistes caeruleus, N = 529) and great tits (Parus major, N = 443). Our samples were collected between autumn and spring, along an elevational gradient in the French Pyrenees and over a three‐year period. Most parasites were found to infect both host species, and while these generalist parasites displayed similar elevational patterns of prevalence in the two host species, this was not always the case for seasonal prevalence patterns. For example, Leucocytozoon group A parasites showed inverse seasonal prevalence when comparing between the two host species, being highest in winter and spring in blue tits but higher in autumn in great tits. While Plasmodium relictum prevalence was overall lower in spring relative to winter or autumn in both species, spring prevalence was also lower in blue tits than in great tits. Together, these results reveal how generalist parasites can exhibit host‐specific epidemiology, which is likely to complicate predictions of host–parasite co‐evolution.     

Linking individual foraging behavior and population spatial distribution in patchy environments: a field example with Mediterranean blue tits

 In spite of recent theoretical interest, few field studies have addressed the links between individual behavioral decisions and population distribution. This work analyzes the foraging behavior of individuals and the spatial distribution of a population of blue tits (Parus caeruleus) just before the main breeding season, when blue tit foraging was not affected by central-place or flocking behaviors. The study was carried out in open holm oak Quercus ilex woodlands (dehesas) that are patchy for canopy-foraging birds because of the scattered arrangement of trees. Residence time on each tree was not correlated either with previous flight time or with prey abundance in trees. Flight distances between trees were larger than average distances estimated in random samples of holm oaks taken close to foraging birds. Trees were not selected by birds on the basis of their expected energy costs and rewards. Bird abundance was not related to food availability in trees or to tree size across dehesas. However, bird abundance was strongly correlated with tree density and with the availability of tree holes for nesting, to the extent that the proportion of tits matched the proportions of both tree abundance and hole abundance across study plots. Overall, neither the behavior of individuals nor the distribution of the population of blue tits corresponded with food resources, which appeared superabundant; instead, tits appeared to behave and be distributed according to the distribution of structural resources such as trees and tree holes for nesting. Received: 18 August 1996 / Accepted: 14 March 1997     

Seasonal variation in reproductive success and post-nuptial moult of blue tits in southern Europe: an experimental study

Post-nuptial moult and reproductive success were studied in relation to timing of breeding in blue tits, Parus caeruleus, breeding in southern Europe. A group of experimentally delayed pairs was created by removing first clutches, thereby inducing late repeat clutches. Reproductive success and post-nuptial moult of delayed pairs were compared with both control pairs that bred early and unmanipulated late-breeding pairs. Delayed pairs fledged fewer young and with a lower body mass than control pairs. However, the number of fledged young and fledgling mass did not differ between delayed and late-breeding pairs. These results were more consistent with the date hypothesis, and it is concluded that the timing of breeding and reproductive success may be causally related in the blue tit. This study reveals a harmful effect of relaying on female body mass at the end of the nestling period. Therefore, females apparently pay the costs of relaying, since a reduction in body mass during the nestling period may be accompanied by a lowered survival probability. Delayed and late-breeding males often began moulting while still feeding young, but neither control males nor females from the three study groups did so. These results support the view that timing-related energy constraints on breeding may be important causes of a seasonal decline in reproductive success at different latitudes. Received: 15 March 1999 / Accepted: 19 July 1999     

Differences in parasite susceptibility and costs of resistance between naturally exposed and unexposed host populations

It is generally assumed that resistance to parasitism entails costs. Consequently, hosts evolving in the absence of parasites are predicted to invest less in costly resistance mechanisms than hosts consistently exposed to parasites. This prediction has, however, rarely been tested in natural populations. We studied the susceptibility of three naïve, three parasitized and one recently isolated Asellus aquaticus isopod populations to an acanthocephalan parasite. We found that parasitized populations, with the exception of the isopod population sympatric with the parasite strain used, were less susceptible to the parasite than the naïve populations. Exposed but uninfected (resistant) isopods from naïve populations, but not from parasitized populations, exhibited greater mortality than controls, implying that resistance entails survival costs primarily for naïve isopods. These results suggest that parasites can drive the evolution of host resistance in the wild, and that co‐existence with parasites may increase the cost‐effectiveness of defence mechanisms.