Continental-scale patterns of pathogen prevalence: a case study on the corncrake

Pathogen infections can represent a substantial threat to wild populations, especially those already limited in size. To determine how much variation in the pathogens observed among fragmented populations is caused by ecological factors, one needs to examine systems where host genetic diversity is consistent among the populations, thus controlling for any potentially confounding genetic effects. Here, we report geographic variation in haemosporidian infection among European populations of corncrake. This species now occurs in fragmented populations, but there is little genetic structure and equally high levels of genetic diversity among these populations. We observed a longitudinal gradient of prevalence from western to Eastern Europe negatively correlated with national agricultural yield, but positively correlated with corncrake census population sizes when only the most widespread lineage is considered. This likely reveals a possible impact of local agriculture intensity, which reduced host population densities in Western Europe and, potentially, insect vector abundance, thus reducing the transmission of pathogens. We conclude that in the corncrake system, where metapopulation dynamics resulted in variations in local census population sizes, but not in the genetic impoverishment of these populations, anthropogenic activity has led to a reduction in host populations and pathogen prevalence

Bat flies (Diptera: Nycteribiidae and Streblidae) infesting cave-dwelling bats in Gabon: Diversity, dynamics and potential role in Polychromophilus melanipherus transmission

Background Evidence of haemosporidian infections in bats and bat flies has motivated a growing interest in characterizing their transmission cycles. In Gabon (Central Africa), many caves house massive colonies of bats that are known hosts of Polychromophilus Dionisi parasites, presumably transmitted by blood-sucking bat flies. However, the role of bat flies in bat malaria transmission remains under-documented. Methods An entomological survey was carried out in four caves in Gabon to investigate bat fly diversity, infestation rates and host preferences and to determine their role in Polychromophilus parasite transmission. Bat flies were sampled for 2–4 consecutive nights each month from February to April 2011 (Faucon and Zadie caves) and from May 2012 to April 2013 (Kessipoughou and Djibilong caves). Bat flies isolated from the fur of each captured bat were morphologically identified and screened for infection by haemosporidian parasites using primers targeting the mitochondrial cytochrome b gene. Results Among the 1,154 bats captured and identified as Miniopterus inflatus Thomas (n = 354), Hipposideros caffer Sundevall complex (n = 285), Hipposideros gigas Wagner (n = 317), Rousettus aegyptiacus Geoffroy (n = 157, and Coleura afra Peters (n = 41), 439 (38.0 %) were infested by bat flies. The 1,063 bat flies recovered from bats belonged to five taxa: Nycteribia schmidlii scotti Falcoz, Eucampsipoda africana Theodor, Penicillidia fulvida Bigot, Brachytarsina allaudi Falcoz and Raymondia huberi Frauenfeld group. The mean infestation rate varied significantly according to the bat species (ANOVA, F (4,75) = 13.15, P < 0.001) and a strong association effect between bat fly species and host bat species was observed. Polychromophilus melanipherus Dionisi was mainly detected in N. s. scotti and P. fulvida and less frequently in E. africana, R. huberi group and B. allaudi bat flies. These results suggest that N. s. scotti and P. fulvida could potentially be involved in P. melanipherus transmission among cave-dwelling bats. Sequence analysis revealed eight haplotypes of P. melanipherus. Conclusions This work represents the first documented record of the cave-dwelling bat fly fauna in Gabon and significantly contributes to our understanding of bat fly host-feeding behavior and their respective roles in Polychromophilus transmission. (Résumé d'auteur

Haemosporidian parasites of Antelopes and other vertebrates from Gabon, Central Africa

Re-examination, using molecular tools, of the diversity of haemosporidian parasites (among which the agents of human malaria are the best known) has generally led to rearrangements of traditional classifications. In this study, we explored the diversity of haemosporidian parasites infecting vertebrate species (particularly mammals, birds and reptiles) living in the forests of Gabon (Central Africa), by analyzing a collection of 492 bushmeat samples. We found that samples from five mammalian species (four duiker and one pangolin species), one bird and one turtle species were infected by haemosporidian parasites. In duikers (from which most of the infected specimens were obtained), we demonstrated the existence of at least two distinct parasite lineages related to Polychromophilus species (i. e., bat haemosporidian parasites) and to sauropsid Plasmodium (from birds and lizards). Molecular screening of sylvatic mosquitoes captured during a longitudinal survey revealed the presence of these haemosporidian parasite lineages also in several Anopheles species, suggesting a potential role in their transmission. Our results show that, differently from what was previously thought, several independent clades of haemosporidian parasites (family Plasmodiidae) infect mammals and are transmitted by anopheline mosquitoes

The polyphyly of Plasmodium: Comprehensive phylogenetic analyses of the malaria parasites (Order Haemosporida) reveal widespread taxonomic conflict

© 2018 The Authors. The evolutionary relationships among the apicomplexan blood pathogens known as the malaria parasites (order Haemosporida), some of which infect nearly 200 million humans each year, has remained a vexing phylogenetic problem due to limitations in taxon sampling, character sampling and the extreme nucleotide base composition biases that are characteristic of this clade. Previous phylogenetic work on the malaria parasites has often lacked sufficient representation of the broad taxonomic diversity within the Haemosporida or the multi-locus sequence data needed to resolve deep evolutionary relationships, rendering our understanding of haemosporidian lifehistory evolution and the origin of the human malaria parasites incomplete. Here we present the most comprehensive phylogenetic analysis of the malaria parasites conducted to date, using samples from a broad diversity of vertebrate hosts that includes numerous enigmatic and poorly known haemosporidian lineages in addition to genome-wide multi-locus sequence data. We find that if base composition differences were corrected for during phylogenetic analysis, we recovered a well-supported topology indicating that the evolutionary history of the malaria parasites was characterized by a complex series of transitions in life-history strategies and host usage. Notably we find that Plasmodium, the malaria parasite genus that includes the species of human medical concern, is polyphyletic with the life-history traits characteristic of this genus having evolved in a dynamic manner across the phylogeny. We find support for multiple instances of gain and loss of asexual proliferation in host blood cells and production of haemozoin pigment, two traits that have been used for taxonomic classification as well as considered to be important factors for parasite virulence and used as drug targets. Lastly, our analysis illustrates the need for a widespread reassessment of malaria parasite taxonomy

Adaptive molecular evolution and biodiversity in malaria parasites

Haemosporidian parasites are the agents of malaria. Countless vertebrates are affected by haemosporidians each year. Haemosporidians have been shown to be evolving at rapid rates; leading to new species of haemosporidians being discovered and new host associations being made. Adaptive molecular evolution was detected in an important hemoglobin degradation gene, falcilysin. At multiple sites across multiple genes involved in important functions signatures of negative selection were detected. The signatures of selection across non-hemoglobin degradation genes were indicative of evolutionary conservation when compared to the more variable hemoglobin degradation genes. This is probably due to the important role the hemoglobin degradation genes play in haemosporidian metabolism. A survey of local passerines detected a parasite prevalence rate of 57%. This included three genera of haemosporidians detected across six lineages and two more distantly related sequences. Leucocytozoon was detected for the first time in Mississippi songbirds, indicating the importance of surveying for understanding haemosporidian evolution and range

FREQUENCY OF AVIAN HAEMOSPORIDIAN PARASITES IN BIRDS FROM MARGARITA AND COCHE ISLANDS, VENEZUELA

By amplifying and sequencing a mitochondrial DNA barcode (cytb), we screened the frequency of haemosporidian parasites (Haemoproteus, Plasmodium, Leucocytozoon) in 366 birds (23 species) from Margarita and Coche islands, Venezuela. In Coche (N = 24), none of the birds were infected, while in Margarita (N = 342) 13 individuals were (3.8%). The frequency of these parasites in endemic bird subspecies was more than double than in non-endemic forms (endemics = 7.3% vs non-endemic = 3.1%, N = 342), but it was not statistically significant. We found eight parasite lineages, four of which are novel (COLPAS09, COLSQU03, COLSQU04, HYPRUF01). COLSQU03, recorded in a dove (Columbina squammata), falls within the Haemoproteus (Parahaemoproteus) subgenus. This was unexpected because a strong signal of co-speciation has been found between Columbidae and the Haemoproteus (Haemoproteus) subgenus, suggesting a host-switching event

Co- and mixed-infections of avian haemosporidian parasites in great tits and blue tits of the French Pyrenees

Avian haemosporidia have played a significant role in advancing our understanding of vectored disease epidemiology, and continue to do so. These diverse blood parasites (inclusive of those responsible for avian malaria) are globally distributed, adopt both host-generalist and host-specialist infection strategies, and can be highly pathogenic. Due the diversity of haemosporidia, many avian populations play host to species rich communities of blood parasites. Interactions between parasites coinfecting a single host can lead to increased pathological costs, between-parasite competition may additionally influence spatial and/or temporal parasite distributions. However, many questions remain regarding the implications of these parasite-parasite interactions and their relevance in nature. In this thesis, I study three genera of avian haemosporidia (Haemoproteus, Leucocytozoon, and Plasmodium) which form a community infecting two geographically overlapping host species, blue tits (Cyanistes caeruleus) and great tits (Parus major). In chapter one, I apply a novel-PCR detection method, which improves the sensitivity of such techniques, to survey the complete local haemosporidian community infecting these birds. Leucocytozoon is the most prevalent genus, infecting >90% of individuals. I identify a significant negative association between Leucocytozoon and Haemoproteus spp., which exists despite similar spatial distributions. An interaction is also identified between two clades of Leucocytozoon, Clade A and Clade D, as mixed-infections are lower than predicted. In chapter two, I further explore this Leucocytozoon clade interaction. Clade A is more prevalent in great tits, while Clade D more prevalent in blue tits, neither impact reproductive measures in their typical host. Clade A has lower prevalence in blue tits, but does carry reproductive costs. Blue tits which have Clade D infections are less likely to be infected by Clade A, which implies a conferred resistance against this great tit-typical parasite. Collectively, these studies reveal complex interactions occurring within a multi-host, multi-parasite community which have important implications for haemosporidia epidemiology and parasite-host co-evolution

Haemosporidian parasite prevalence, parasitemia, and diversity in three resident bird species at a shrubland dominated landscape of the Mexican highland plateau

"Background: Studies of avian haemosporidians allow understanding how these parasites affect wild bird populations, and if their presence is related to factors such as habitat loss, degradation and fragmentation, and climate change. Considering the importance of the highland Plateau of Mexico as part of the North American bird migratory route and as a region containing important habitat for numerous bird species, the purpose of this study was to document haemosporidian species richness and how habitat degradation, bird body condition, and distance from water sources correlate with bird parasitemia. Methods: We assessed the presence of avian haemosporidians in three resident bird species through microscopy and PCR amplification of a fragment of the haemosporidian cytochrome b gene. Average parasitemia was estimated in each species, and its relationship with habitat degradation through grazing, bird body condition and distance from water bodies was assessed. Results: High levels of parasitemia were recorded in two of the three bird species included in this study. Four lineages of haemosporidians were identified in the study area with nearly 50 % prevalence. Areas with highly degraded shrublands and villages showed higher parasitemia relative to areas with moderately degraded shrublands. No strong relationship between parasitemia and distance from water bodies was observed. There were no significant differences in prevalence and parasitemia between the two bird species infected with the parasites. Two of the sequences obtained from the fragments of the parasite's cytochrome b gene represent a lineage that had not been previously reported. Conclusions: Haemosporidian diversity in arid zones of the Mexican highland plateau is high. Shrubland habitat degradation associated to the establishment of small villages, as well as tree extraction and overgrazing in the surroundings of these villages, significantly enhances parasitemia of birds by haemosporidians.

Avian haemosporidian infections in rufous-collared sparrows in an Andean dry forest: diversity and factors related to prevalence and parasitaemia

Despite intensive research during the last few decades, understanding of ecological and physiological factors related to haemosporidian infections in birds is still fragmentary. Since more model organisms are needed in order to understand these infections in the wild, we analysed avian haemosporidian infections in the rufous-collared sparrow (Zonotrichia capensis, Emberizidae) in a dry forest of the Ecuadorian Andes. Parasite diversity was screened using molecular and morphological approaches. By molecular diagnosis, we identified three linages that were phylogenetically placed in the context of molecular haemosporidian diversity and associated with a morphospecies. By microscopy, we identified five described morphospecies and one additional undescribed morphospecies. We found that avian haemosporidian prevalence on the study site was 76.3%. Additionally, we used a series of generalized linear models to explore the potential relationship of parasite prevalence and parasitaemia with a set of variables related to physiological and environmental conditions. Although our results revealed associations of haemosporidian infections with precipitation, age and sampling site, the models only explained a small fraction of the variation