The evolution of virulence and host specialization in malaria parasites of primates

Parasite virulence, i.e. the damage done to the host, may be a by-product of the parasite's effort to maximize its fitness. Accordingly, several life-history trade-offs may explain interspecific differences in virulence, but such constraints remain little tested in an evolutionary context. In this phylogenetic study of primate malarias, I investigated the relationship between virulence and other parasite life-history traits. I used peak parasitaemia as a proxy for virulence, because it reflected parasite reproductive success and parasite-induced mortality. Peak parasitaemia was higher in specialist than in generalist species, even when confounding life-history traits were controlled. While there was a significant phylogenetic relationship between the number of competitors per host and host specialization, peak parasitaemia was unrelated to within-host competition. Therefore, the key evolutionary factor that favours virulence is host specialization, and the evolutionary success of virulent parasites, such as Plasmodium falciparum , may be better understood when the trade-off in virulence between different hosts is considered. Such phylogenetic results may help us design better protection programmes against malaria.     

Resource predictability and specialization in avian malaria parasites

We tested the hypothesis that avian haemosporidian (malaria) parasites specialize on hosts that can be characterized as predictable resources at a site in Amazonian Ecuador. We incorporated host phylogenetic relationship and relative abundance in assessing parasite specialization, and we examined associations between parasite specialization and three host characteristics – abundance, mass and longevity – using quantile regression, phylogenetic logistic regression and t‐tests. Hosts of specialist malaria parasite lineages were on average more abundant than hosts of generalist parasite lineages, but the relationship between host abundance and parasite specialization was not consistent across analyses. We also found support for a positive association between parasite specialization and host longevity, but this also was not consistent across analyses. Nonetheless, our findings suggest that the predictability of a host resource may play a role in the evolution of specialization. However, we also discuss two alternative explanations to the resource predictability hypothesis for specialization: (i) that interspecific interactions among the parasites themselves might constrain some parasites to a specialist strategy, and (ii) that frequent encounters with multiple host species, mediated by blood‐sucking insects, might promote generalization within this system.     

Sex-biased,but not plumage color-based,prevalence of haemosporidian parasites in free-range chickens

Previous studies found a relationship between blood parasite infection and bird gender, with higher prevalence in males. Some studies also found a relationship between host plumage color and parasitic infection, while others did not. Here, we investigated the blood parasite prevalence in correlation with sex and plumage color in free-range chickens (Gallus gallus domesticus) in China. We analyzed a total of 297 blood samples, out of which 234 chickens tested positive for haemosporidian parasites, with 78.5% parasite prevalence. Out of 139 males, 118 tested positive with 84.8% parasite prevalence while 116 of 158 female samples tested positive (73.4%). Leucocytotozoon was the most frequent genus isolated (193 infected individuals /234 birds), followed by Plasmodium (41 infected individuals/234 birds), with no Haemoproteus parasites being detected. There were no significant differences in the body parameters and chicken color plumages with regards to the infection status. Our study indicated that blood parasite infection was significantly different between male and female chickens, with infection prevalent in males.     

Migratory birds have higher prevalence and richness of avian haemosporidian parasites than residents

Individuals of migratory species may be more likely to become infected by parasites because they cross different regions along their route, thereby being exposed to a wider range of parasites during their annual cycle. Conversely, migration may have a protective effect since migratory behaviour allows hosts to escape environments presenting a high risk of infection. Haemosporidians are one of the best studied, most prevalent and diverse groups of avian parasites, however the impact of avian host migration on infection by these parasites remains controversial. We tested whether migratory behaviour influenced the prevalence and richness of avian haemosporidian parasites among South American birds. We used a dataset comprising ~ 11,000 bird blood samples representing 260 bird species from 63 localities and Bayesian multi-level models to test the impact of migratory behaviour on prevalence and lineage richness of two avian haemosporidian genera (Plasmodium and Haemoproteus). We found that fully migratory species present higher parasite prevalence and higher richness of haemosporidian lineages. However, we found no difference between migratory and non-migratory species when evaluating prevalence separately for Plasmodium and Haemoproteus, or for the richness of Plasmodium lineages. Nevertheless, our results indicate that migratory behaviour is associated with an infection cost, namely a higher prevalence and greater variety of haemosporidian parasites.     

Loss of forest cover and host functional diversity increases prevalence of avian malaria parasites in the Atlantic Forest

Host phylogenetic relatedness and ecological similarity are thought to contribute to parasite community assembly and infection rates. However, recent landscape level anthropogenic changes may disrupt host-parasite systems by impacting functional and phylogenetic diversity of host communities. We examined whether changes in host functional and phylogenetic diversity, forest cover, and minimum temperature influence the prevalence, diversity, and distributions of avian haemosporidian parasites (genera Haemoproteus and Plasmodium) across 18 avian communities in the Atlantic Forest. To explore spatial patterns in avian haemosporidian prevalence and taxonomic and phylogenetic diversity, we surveyed 2241 individuals belonging to 233 avian species across a deforestation gradient. Mean prevalence and parasite diversity varied considerably across avian communities and parasites responded differently to host attributes and anthropogenic changes. Avian malaria prevalence (termed herein as an infection caused by Plasmodium parasites) was higher in deforested sites, and both Plasmodium prevalence and taxonomic diversity were negatively related to host functional diversity. Increased diversity of avian hosts increased local taxonomic diversity of Plasmodium lineages but decreased phylogenetic diversity of this parasite genus. Temperature and host phylogenetic diversity did not influence prevalence and diversity of haemosporidian parasites. Variation in the diversity of avian host traits that promote parasite encounter and vector exposure (host functional diversity) partially explained the variation in avian malaria prevalence and diversity. Recent anthropogenic landscape transformation (reduced proportion of native forest cover) had a major influence on avian malaria occurrence across the Atlantic Forest. This suggests that, for Plasmodium, host phylogenetic diversity was not a biotic filter to parasite transmission as prevalence was largely explained by host ecological attributes and recent anthropogenic factors. Our results demonstrate that, similar to human malaria and other vector-transmitted pathogens, prevalence of avian malaria parasites will likely increase with deforestation.     

The relationship between specialization and local abundance: the case of helminth parasites of birds

Positive relationships are commonly observed between the abundance of a species in a locality and the frequency of its occurrence among localities on a larger scale. This pattern may not hold for parasitic organisms when the average abundance of a parasite among its hosts is related to the number of host species in which it occurs, because of the additive investment in specific adaptations to counter host immune responses required for each host species in a parasites repertoire. For a rigorous test of the hypothesis that there is a trade-off between the number of host species that can be successfully exploited and the average abundance of parasites in those hosts, one needs to take into account the phylogenetic (or taxonomic) distances among the host species used by a parasite. Differences in immune responses are likely to increase with increasing phylogenetic distances. The trade-off hypothesis was tested in a comparative analysis of 393 species of trematodes, cestodes and nematodes parasitic in birds surveyed from the same geographical area, using an index of host specificity that measures the average taxonomic distances between a parasites known host species. After correcting for the influences of parasite phylogeny and other potential confounding variables, mean abundance was negatively correlated with the average taxonomic distance among host species for nematodes, and with the variance in taxonomic distances among hosts for cestodes. In the case of trematodes, these variables covaried positively. The trade-off between average infection success and how taxonomically distant a parasites host species are from each other was only found in two of the three groups of helminths investigated, possibly because of compensating features in trematodes, such as their ability to multiply asexually in intermediate hosts. These results provide empirical evidence consistent with the hypothesis that specialization allows greater local adaptation and therefore greater local population abundance, supporting key predictions regarding the evolution of ecological specialization.Electronic Supplementary Material Supplementary material is available for this article at     

Avian host composition,local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds

Identifying the ecological factors that shape parasite distributions remains a central goal in disease ecology. These factors include dispersal capability, environmental filters and geographic distance. Using 520 haemosporidian parasite genetic lineages recovered from 7,534 birds sampled across tropical and temperate South America, we tested (a) the latitudinal diversity gradient hypothesis and (b) the distance–decay relationship (decreasing proportion of shared species between communities with increasing geographic distance) for this host–parasite system. We then inferred the biogeographic processes influencing the diversity and distributions of this cosmopolitan group of parasites across South America. We found support for a latitudinal gradient in diversity for avian haemosporidian parasites, potentially mediated through higher avian host diversity towards the equator. Parasite similarity was correlated with climate similarity, geographic distance and host composition. Local diversification in Amazonian lineages followed by dispersal was the most frequent biogeographic events reconstructed for haemosporidian parasites. Combining macroecological patterns and biogeographic processes, our study reveals that haemosporidian parasites are capable of circumventing geographic barriers and dispersing across biomes, although constrained by environmental filtering. The contemporary diversity and distributions of haemosporidian parasites are mainly driven by historical (speciation) and ecological (dispersal) processes, whereas the parasite community assembly is largely governed by host composition and to a lesser extent by environmental conditions.     

Moderate transmission but high prevalence of malaria in Madagascar

Malaria transmission remains poorly documented in areas of low transmission. A study has been carried out over two consecutive years in Analamiranga, a village located at an altitude of 885m on the western edge of the Malagasy highlands, with the aim of generating and updating malariometric indexes for both mosquitoes and schoolchildren. In this village, no vector control measures were performed during the study period nor during previous decades. Mosquitoes were collected monthly when landing on human volunteers and in various resting-places. Blood samples were taken every 3 months from schoolchildren aged 6-12 years and microscopically examined. Of 7,480 mosquitoes collected on human subjects, 5,790 were anophelines. Ten anopheline species were represented and three of these, Anopheles funestus, Anopheles arabiensis and Anopheles mascarensis, accounted for 59.2% of the collection. Of these three species 4,640 were also collected in resting places. The proportion of mosquitoes fed on bovids was high; conversely, the anthropophilic rate (mosquitoes fed on human beings) was especially low: 31%, 7% and 1%, respectively, for A. funestus, A. arabiensis and A. mascarensis. The only confirmed malaria vector was A. funestus with a low sporozoite index (of 6,830 A. funestus, five were positive for Plasmodium falciparum and four for Plasmodium vivax). The annual entomological inoculation rate (number of bites of infected anophelines per adult person) was estimated at 2.49 with low variation over the 2 years. Overall, 909 thick blood smears were tested from blood samples taken from schoolchildren with 30.3% being malaria-positive. The four Plasmodium species infecting human subjects were detected in the following proportions: P. falciparum 78.9%, P. vivax 19.4%, Plasmodium malariae 1.0% and Plasmodium ovale 0.7%. The proportions of children who were infected with any Plasmodium ranged from 10.7% in February to 51.0% in September. Parasitemic children with fever (axillary temperature >37.5 degrees C) accounted for 16.4% of the children sampled. This study demonstrates that there are substantial parasitological consequences of even a relatively low entomological transmission and also recommends including exterior resting-places of mosquitoes in future spraying campaigns in the highlands of Madagascar.     

Prevalence of malaria and related haemosporidian parasites in two shorebird species with different winter habitat distribution

Parasites can have strong effects on host life-history and behaviour, and result in changes in host population dynamics and community structure. We applied a PCR-based technique and examined prevalence of malaria and related haemosporidian parasites in two arctic breeding shorebird species: the Semipalmated Sandpiper (Calidris pusilla) and the Pectoral Sandpiper (C. melanotos). During the non-breeding season, Semipalmated Sandpipers inhabit coastal marine habitats, whereas Pectoral Sandpipers are found in inland areas. In accordance with the hypothesis that the risk of parasite infection is higher in a species wintering in freshwater areas, we found Plasmodium sp. infection during the breeding season only in Pectoral Sandpipers, whereas Semipalmated Sandpipers were parasite free. However, even in Pectoral Sandpipers sampled in the arctic, prevalence of malaria parasites was very low (<3% of individuals, n = 114). Overall, three different Plasmodium sp. lineages were found, one of which has never been described before.     

Host specificity of avian haemosporidian parasites is unrelated among sister lineages but shows phylogenetic signal across larger clades

Parasites can vary in the number of host species they infect, a trait known as “host specificity”. Here we quantify phylogenetic signal—the tendency for closely related species to resemble each other more than distantly related species—in host specificity of avian haemosporidian parasites (genera Plasmodium, Haemoproteus and Leucocytozoon) using data from MalAvi, the global avian haemosporidian database. We used the genetic data (479 base pairs of cytochrome b) that define parasite lineages to produce genus level phylogenies. Combining host specificity data with those phylogenies revealed significant levels of phylogenetic signal while controlling for sampling effects; phylogenetic signal was higher when the phylogenetic diversity of hosts was taken into account. We then tested for correlations in the host specificity of pairs of sister lineages. Correlations were generally close to zero for all three parasite genera. These results suggest that while the host specificity of parasite sister lineages differ, larger clades may be relatively specialised or generalised.     

Avian host community structure and prevalence of West Nile virus in Chicago,Illinois

Vertebrate host diversity has been postulated to mediate prevalence of zoonotic, vector-borne diseases, such that as diversity increases, transmission dampens. This “dilution effect” is thought to be caused by distribution of infective bites to incompetent reservoir hosts. We quantified avian species richness, avian seroprevalence for antibodies to West Nile virus (WNV), and infection of WNV in Culex mosquitoes, in the Chicago metropolitan area, Illinois, USA, a region of historically high WNV activity. Results indicated high overall avian seroprevalence and variation in seroprevalence across host species; however, there was no negative correlation between avian richness and Culex infection rate or between richness and infection status in individual birds. Bird species with high seroprevalence, especially northern cardinals and mourning doves, may be important sentinels for WNV in Chicago, since they were common and widespread among all study sites. Overall, our results suggest no net effect of increasing species richness to West Nile virus transmission in Chicago. Other intrinsic and extrinsic factors, such as variation in mosquito host preference, reservoir host competence, temperature, and precipitation, may be more important than host diversity for driving interannual variation in WNV transmission. These results from a fine-scale study call into question the generality of a dilution effect for WNV at coarser spatial scales.     

黑龙江凉水和丰林保护区鸟类和兽类多样性

2013年12月至2015年5月、2014年4月至2015年5月利用红外相机分别对黑龙江凉水保护区和丰林保护区鸟兽多样性进行研究:凉水保护区累计10736个捕获日,获得有效照片总数14726张,兽类独立照片514张,共4目7科11种,鸟类独立照片107张,共4目8科11种;丰林保护区累计7460个捕获日,获得有效照片总数13677张,兽类独立照片638张,共3目6科9种,鸟类独立照片166张,共4目10科16种。凉水保护区实际监测到的鸟兽物种数约为全部鸟兽物种的70%—78%;丰林保护区实际监测到的鸟兽物种数目全部鸟兽物种的80%—89%,保护区内大部分物种被监测到。凉水和丰林保护区兽类相对丰富度最高的均为松鼠(Sciurus vulgaris)和花鼠(Eutamias sibiricus),其次为西伯利亚狍(Capreolus capreolu),鸟类相对丰富度最高的普通鳾(Sitta europaea)和白腹鸫(Turdus pallidus);物种多样性指数显示鸟兽多样性无显著差异;鸟、兽群落相似性指数Cs=0.621,凉水和丰林保护区鸟兽物种有较多重叠。利用红外相机对凉水和丰林保护区鸟兽多样性进行研究发现,兽类中对夜行性小型啮齿类监测不足,监测到的鸟类以林下活动为主。     

Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles

We recovered 26 genetically distinct avian malaria parasite lineages, based on cytochrome b sequences, from a broad survey of terrestrial avifauna of the Lesser Antilles. Here we describe their distributions across host species within a regional biogeographic context. Most parasite lineages were recovered from a few closely related host species. Specialization on one host species and distribution across many hosts were both rare. Geographic patterns of parasite lineages indicated limited dispersal and frequent local extinction. The central islands of the archipelago share similar parasite lineages and patterns of infection. However, the peripheral islands harbor well-differentiated parasite communities, indicating long periods of isolation. Nonetheless, 20 of 26 parasite lineages were recovered from at least one of three other geographic regions, the Greater Antilles, North America, and South America, suggesting rapid dispersal relative to rate of differentiation. Six parasite lineages were restricted to the Lesser Antilles, primarily to endemic host species. Host differences between populations of the same parasite lineage suggest that host preference may evolve more rapidly than mitochondrial gene sequences. Taken together, distributions of avian malarial parasites reveal evidence of coevolution, host switching, extinction, and periodic recolonization events resulting in ecologically dynamic as well as evolutionarily stable patterns of infection.     

The prevalence of avian haemosporidian parasites in an invasive bird is lower in urban than in non-urban environments

Urbanization affects the ecology of wildlife diseases and although it has been suggested that there are lower risks of infection in urban areas, there have been no experiments to support this conclusion. We assessed haemosporidian prevalence and intensity in House Sparrows Passer domesticus using field and experimental data under contrasting conditions (i.e. urban vs. non-urban). For experimental data, we kept 32 male House Sparrows in captivity as a proxy of stress, and for field data we sampled 49 House Sparrows (17 females). We made use of microscopy to determine the relative intensity and used the polymerase chain reaction to estimate infection prevalence. We obtained total leucocyte counts, leucocyte differentials, heterophil/lymphocyte ratio (H/L) as a measure of stress, and the Polychromatic Index as a measure of physiological condition (erythropoiesis). We identified a total of 10 haemosporidian lineages. For field samples (both males and females), we found a significantly higher prevalence of infection in non-urban House Sparrows than in urban ones. Under experimental conditions, non-urban House Sparrows showed a higher prevalence than urban ones both before and after captivity, with a significant increase in parasite intensity. The number of infected birds increased after captivity for both urban (~ 32%) and non-urban House Sparrows (~ 19%), indicating either a recrudescence of chronic and relapses of latent infections or the appearance of infections that had been acquired earlier. The H/L ratio was significantly higher for non-urban than for urban male House Sparrows before captivity. No difference in H/L was found for urban House Sparrows before and after captivity, indicating tolerance to city stressors. Our results showed a significant decrease in H/L for non-urban birds after captivity, suggesting higher stress in the non-urban agricultural environment. Haemosporidian infections were not associated with the H/L ratio. Our study provides evidence that highly urbanized areas within cities represent lower haemosporidian infection risks than do non-urban areas for House Sparrows.     

Robust geographical determinants of infection prevalence and a contrasting latitudinal diversity gradient for haemosporidian parasites in Western Palearctic birds

Identifying robust environmental predictors of infection probability is central to forecasting and mitigating the ongoing impacts of climate change on vector‐borne disease threats. We applied phylogenetic hierarchical models to a data set of 2,171 Western Palearctic individual birds from 47 species to determine how climate and landscape variation influence infection probability for three genera of haemosporidian blood parasites (Haemoproteus, Leucocytozoon, and Plasmodium). Our comparative models found compelling evidence that birds in areas with higher vegetation density (captured by the normalized difference vegetation index [NDVI]) had higher likelihoods of carrying parasite infection. Magnitudes of this relationship were remarkably similar across parasite genera considering that these parasites use different arthropod vectors and are widely presumed to be epidemiologically distinct. However, we also uncovered key differences among genera that highlighted complexities in their climate responses. In particular, prevalences of Haemoproteus and Plasmodium showed strong but contrasting relationships with winter temperatures, supporting mounting evidence that winter warming is a key environmental filter impacting the dynamics of host‐parasite interactions. Parasite phylogenetic community diversities demonstrated a clear but contrasting latitudinal gradient, with Haemoproteus diversity increasing towards the equator and Leucocytozoon diversity increasing towards the poles. Haemoproteus diversity also increased in regions with higher vegetation density, supporting our evidence that summer vegetation density is important for structuring the distributions of these parasites. Ongoing variation in winter temperatures and vegetation characteristics will probably have far‐reaching consequences for the transmission and spread of vector‐borne diseases.