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1.
Infect Immun ; 92(1): e0024423, 2024 Jan 16.
Article in English | MEDLINE | ID: mdl-38099660

ABSTRACT

Interactions among pathogen genotypes that vary in host specificity may affect overall transmission dynamics in multi-host systems. Borrelia burgdorferi, a bacterium that causes Lyme disease, is typically transmitted among wildlife by Ixodes ticks. Despite the existence of many alleles of B. burgdorferi's sensu stricto outer surface protein C (ospC) gene, most human infections are caused by a small number of ospC alleles ["human infectious alleles" (HIAs)], suggesting variation in host specificity associated with ospC. To characterize the wildlife host association of B. burgdorferi's ospC alleles, we used metagenomics to sequence ospC alleles from 68 infected individuals belonging to eight mammalian species trapped at three sites in suburban New Brunswick, New Jersey (USA). We found that multiple allele ("mixed") infections were common. HIAs were most common in mice (Peromyscus spp.) and only one HIA was detected at a site where mice were rarely captured. ospC allele U was exclusively found in chipmunks (Tamias striatus), and although a significant number of different alleles were observed in chipmunks, including HIAs, allele U never co-occurred with other alleles in mixed infections. Our results suggest that allele U may be excluding other alleles, thereby reducing the capacity of chipmunks to act as reservoirs for HIAs.


Subject(s)
Borrelia burgdorferi , Borrelia , Coinfection , Ixodes , Lyme Disease , Animals , Humans , Borrelia burgdorferi/genetics , Borrelia/genetics , Alleles , Lyme Disease/microbiology , Ixodes/genetics , Ixodes/microbiology , Antigens, Bacterial/genetics , Bacterial Outer Membrane Proteins/genetics , Sciuridae/genetics , Host Specificity
2.
G3 (Bethesda) ; 13(8)2023 08 09.
Article in English | MEDLINE | ID: mdl-37130071

ABSTRACT

The clapper rail (Rallus crepitans), of the family Rallidae, is a secretive marsh bird species that is adapted for high salinity habitats. They are very similar in appearance to the closely related king rail (R. elegans), but while king rails are limited primarily to freshwater marshes, clapper rails are highly adapted to tolerate salt marshes. Both species can be found in brackish marshes where they freely hybridize, but the distribution of their respective habitats precludes the formation of a continuous hybrid zone and secondary contact can occur repeatedly. This system, thus, provides unique opportunities to investigate the underlying mechanisms driving their differential salinity tolerance as well as the maintenance of the species boundary between the 2 species. To facilitate these studies, we assembled a de novo reference genome assembly for a female clapper rail. Chicago and HiC libraries were prepared as input for the Dovetail HiRise pipeline to scaffold the genome. The pipeline, however, did not recover the Z chromosome so a custom script was used to assemble the Z chromosome. We generated a near chromosome level assembly with a total length of 994.8 Mb comprising 13,226 scaffolds. The assembly had a scaffold N50 was 82.7 Mb, L50 of four, and had a BUSCO completeness score of 92%. This assembly is among the most contiguous genomes among the species in the family Rallidae. It will serve as an important tool in future studies on avian salinity tolerance, interspecific hybridization, and speciation.


Subject(s)
Ecosystem , Genome , Female , Animals , Wetlands , Birds/genetics
3.
Biol Lett ; 19(3): 20220459, 2023 03.
Article in English | MEDLINE | ID: mdl-36918035

ABSTRACT

Parasite dispersal and host-switching may be better understood by knowing when they occurred. We estimated when the ancestor of a parasite of great reed warblers (Acrocephalus arundinaceus) dispersed to the Seychelles and began infecting the endemic Seychelles warbler (A. sechellensis). We used mitochondrial genomes and published molecular divergence rates to estimate the date of divergence between mitochondrial haplotypes of the parasite Haemoproteus nucleocondensis (lineage GRW01) in the great reed warbler and the Seychelles warbler. We also constructed a time-calibrated phylogeny of the hosts and their relatives to determine when the ancestor of the Seychelles warbler dispersed to the Seychelles. The two GRW01 lineages diverged ca 20-451 kya, long after the ancestor of the Seychelles warbler colonized the Seychelles ca 1.76-4.36 Mya. GRW01 rarely infects other species despite apparent opportunity. Humans were likely not involved in the dispersal of this parasite because humans settled the Seychelles long after the parasite diverged from its mainland relative. Furthermore, introduced birds are unlikely hosts of GRW01. Instead, the ancestor of GRW01 may have dispersed to the Seychelles with an errant migrating great reed warbler. Our results indicate that even specialized parasites can naturally disperse long distances to become emerging infectious diseases.


Subject(s)
Haemosporida , Parasites , Passeriformes , Songbirds , Animals , Humans , Songbirds/genetics , Haemosporida/genetics , Seychelles , Phylogeny
4.
Ticks Tick Borne Dis ; 14(3): 102139, 2023 05.
Article in English | MEDLINE | ID: mdl-36780839

ABSTRACT

Characterizing the diversity of genes associated with virulence and transmission of a pathogen across the pathogen's distribution can inform our understanding of host infection risk. Borrelia burgdorferi is a vector-borne bacterium that causes Lyme disease in humans and is common in the United States. The outer surface protein C (ospC) gene of B. burgdorferi exhibits substantial genetic variation across the pathogen's distribution and plays a critical role in virulence and transmission in vertebrate hosts. In fact, B. burgdorferi infections that disseminate across host tissues in humans are associated with only a subset of ospC alleles. Delaware has a high incidence of Lyme disease, but the diversity of ospC in B. burgdorferi in the state has not been evaluated. We used PCR to amplify ospC in B. burgdorferi-infected blacklegged ticks (Ixodes scapularis) in sites statewide and used short-read sequencing to identify ospC alleles. B. burgdorferi prevalence in blacklegged ticks varied across sites, but not significantly so. We identified 15 previously characterized ospC alleles accounting for nearly all of the expected diversity of alleles across the sites as estimated using the Chao1 index. Nearly 40% of sequenced infections (23/58) had more than one ospC allele present suggesting mixed strain infections and the relative frequencies of alleles in single infections were positively correlated with their relative frequencies in mixed infections. Turnover of ospC alleles was positively related to distance between sites with closer sites having more similar allele compositions than more distant sites. This suggests a degree of B. burgdorferi dispersal limitation or habitat specialization. OspC alleles known to cause disseminated infections in humans were found at the highest frequencies across sites, corresponding to Delaware's high incidence of Lyme disease.


Subject(s)
Borrelia burgdorferi , Ixodes , Lyme Disease , Animals , Humans , Borrelia burgdorferi/genetics , Ixodes/microbiology , Alleles , Prevalence , Delaware , Lyme Disease/epidemiology , Lyme Disease/microbiology
5.
Vet Res Commun ; 47(2): 511-521, 2023 Jun.
Article in English | MEDLINE | ID: mdl-35739341

ABSTRACT

Infections of avian haemosporidian parasites are regularly identified by molecular methods including multiplex PCR, which allows researchers to distinguish mixed infections of parasites from multiple genera. Here we extend the utility of a previously designed multiplex PCR by designing a primer set specific to parasites of the subgenus Haemoproteus (genus: Haemoproteus). The updated one-step multiplex PCR protocol we describe here allows for the detection of the genera Plasmodium and Leucocytozoon and the two subgenera (Haemoproteus and Parahaemoproteus) of the genus Haemoproteus. A sensitivity analysis showed that the multiplex PCR could amplify DNA of parasites in the subgenus Haemoproteus at very low levels of infection. We used this multiplex PCR to identify haemosporidian infections in 250 adult domestic pigeons (Columba livia) in Turkey. All samples were also screened by microscopy and a widely used nested PCR to compare with the results of multiplex PCR, to detect low levels of parasitemia, and to identify possible abortive infections. In total, 71 pigeons (28.4%) were found to be infected by all three methods. The multiplex PCR protocol successfully detected and discriminated both subgenera Haemoproteus and Parahaemoproteus infections. We compared our results with previous host species records to assess the host specificity of the parasite lineages we found. Our findings provide novel data on the prevalence of avian haemosporidians in domestic pigeons and demonstrate the utility of the new one-step multiplex PCR protocol for the determination of mixed avian haemosporidian infections. We expect that this protocol will contribute to a better understanding of the distribution, epizootiology, and ecology of avian haemosporidians.


Subject(s)
Bird Diseases , Haemosporida , Parasites , Protozoan Infections, Animal , Animals , Columbidae/genetics , Columbidae/parasitology , Parasites/genetics , Multiplex Polymerase Chain Reaction/veterinary , Prevalence , Turkey , Protozoan Infections, Animal/diagnosis , Protozoan Infections, Animal/epidemiology , Protozoan Infections, Animal/parasitology , DNA, Protozoan/genetics , Bird Diseases/diagnosis , Bird Diseases/epidemiology , Haemosporida/genetics
6.
Parasit Vectors ; 15(1): 267, 2022 Jul 29.
Article in English | MEDLINE | ID: mdl-35906670

ABSTRACT

BACKGROUND: Sequencing parasite genomes in the presence of host DNA is challenging. Sequence capture can overcome this problem by using RNA probes that hybridize with the parasite DNA and then are removed from solution, thus isolating the parasite DNA for efficient sequencing. METHODS: Here we describe a set of sequence capture probes designed to target 1035 genes (c. 2.5 Mbp) of the globally distributed avian haemosporidian parasite, Plasmodium relictum. Previous sequence capture studies of avian haemosporidians from the genus Haemoproteus have shown that sequencing success depends on parasitemia, with low-intensity, chronic infections (typical of most infected birds in the wild) often being difficult to sequence. We evaluate the relationship between parasitemia and sequencing success using birds experimentally infected with P. relictum and kept under laboratory conditions. RESULTS: We confirm the dependence of sequencing success on parasitemia. Sequencing success was low for birds with low levels of parasitemia (< 1% infected red blood cells) and high for birds with higher levels of parasitemia. Plasmodium relictum is composed of multiple lineages defined by their mitochondrial DNA haplotype including three that are widespread (SGS1, GRW11, and GRW4); the probes successfully isolated DNA from all three. Furthermore, we used data from 25 genes to describe both among- and within-lineage genetic variation. For example, two samples of SGS1 isolated from different host species differed by 11 substitutions across those 25 genes. CONCLUSIONS: The sequence capture approach we describe will allow for the generation of genomic data that will contribute to our understanding of the population genetic structure and evolutionary history of P. relictum, an extreme host generalist and widespread parasite.


Subject(s)
Haemosporida , Malaria, Avian , Plasmodium , Animals , Birds , Genomics , Haemosporida/genetics , Malaria, Avian/parasitology , Parasitemia/parasitology , Parasitemia/veterinary
7.
Malar J ; 20(1): 265, 2021 Jun 12.
Article in English | MEDLINE | ID: mdl-34118950

ABSTRACT

BACKGROUND: Although avian Plasmodium species are widespread and common across the globe, limited data exist on how genetically variable their populations are. Here, the hypothesis that the avian blood parasite Plasmodium relictum exhibits very low genetic diversity in its Western Palearctic transmission area (from Morocco to Sweden in the north and Transcaucasia in the east) was tested. METHODS: The genetic diversity of Plasmodium relictum was investigated by sequencing a portion (block 14) of the fast-evolving merozoite surface protein 1 (MSP1) gene in 75 different P. relictum infections from 36 host species. Furthermore, the full-length MSP1 sequences representing the common block 14 allele was sequenced in order to investigate if additional variation could be found outside block 14. RESULTS: The majority (72 of 75) of the sequenced infections shared the same MSP1 allele. This common allele has previously been found to be the dominant allele transmitted in Europe. CONCLUSION: The results corroborate earlier findings derived from a limited dataset that the globally transmitted malaria parasite P. relictum exhibits very low genetic diversity in its Western Palearctic transmission area. This is likely the result of a recent introduction event or a selective sweep.


Subject(s)
Genetic Variation , Haplotypes , Merozoite Surface Protein 1/genetics , Plasmodium/genetics , Songbirds/parasitology , Animals , Armenia , Morocco , Portugal , Russia
8.
Ticks Tick Borne Dis ; 12(5): 101736, 2021 09.
Article in English | MEDLINE | ID: mdl-33992910

ABSTRACT

The Mediterranean tick, Hyalomma marginatum, is the most important vector of Crimean-Congo haemorrhagic fever virus and several pathogens that cause animal and human diseases and economic losses to livestock production. Given the medical and veterinary importance of this tick species, we sequenced and characterized its mitochondrial genome (mitogenome) for the first time. We designed two new primer sets and combined long-range PCR with next generation sequencing to generate complete mitogenomes with deep coverage from 10 H. marginatum adults. The mitogenomes contained 13 protein-coding genes (PCGs), 22 transfer RNAs (tRNAs), two ribosomal subunits, two control regions, and three tick-box motifs. The nucleotide composition of the H. marginatum mitogenomes were A+T biased (79.76%) and exhibited negative AT- and GC- skews across most PCGs. All PCGs were initiated by ATK codons and two truncated termination codons were seen in the COX2 and COX3 genes. All tRNAs exhibited typical cloverleaf structures, except for tRNACys and tRNASer1. A total of 62 polymorphic sites defined ten unique haplotypes. Phylogenetic analyses based on the 13 PCGs of 56 tick species revealed that four Hyalomma species (H. marginatum, H. asiaticum, H. rufipes, and H. truncatum) formed a monophyletic clade with strong support. The results of this study provide a comprehensive resource for further studies on the systematics, population genetics, molecular epidemiology, and evolution of ticks.


Subject(s)
Genome, Mitochondrial , Ixodidae/genetics , Animals , Arachnid Vectors/genetics , Disease Vectors , Hemorrhagic Fever, Crimean/transmission , High-Throughput Nucleotide Sequencing , Humans , Phylogeny
9.
Int J Parasitol ; 51(9): 719-728, 2021 08.
Article in English | MEDLINE | ID: mdl-33722680

ABSTRACT

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.


Subject(s)
Bird Diseases , Haemosporida , Malaria, Avian , Parasites , Plasmodium , Animals , Bird Diseases/epidemiology , Forests , Haemosporida/genetics , Humans , Malaria, Avian/epidemiology , Phylogeny , Plasmodium/genetics , Prevalence
10.
Mol Phylogenet Evol ; 153: 106947, 2020 12.
Article in English | MEDLINE | ID: mdl-32866615

ABSTRACT

Parasite species evolve by switching to new hosts, cospeciating with their current hosts, or speciating on their current hosts. Vector transmitted parasites are expected to speciate by host switching, but confirming this hypothesis has proved challenging. Parasite DNA can be difficult to sequence, thus well resolved parasite phylogenies that are needed to distinguish modes of parasite speciation are often lacking. Here, we studied speciation in vector transmitted avian haemosporidian parasites in the genus Haemoproteus and their warbler hosts (family Acrocephalidae). We overcome the difficulty of generating parasite genetic data by combining nested long-range PCR with next generation sequencing to sequence whole mitochondrial genomes from 19 parasite haplotypes confined to Acrocephalidae warblers, resulting in a well-supported parasite phylogeny. We also generated a well-supported host phylogeny using five genes from published sources. Our phylogenetic analyses confirm that these parasites have speciated by host switching. We also found that closely related host species shared parasites which themselves were not closely related. Sharing of parasites by closely related host species is not due to host geographic range overlap, but may be the result of phylogenetically conserved host immune systems.


Subject(s)
Genome, Mitochondrial/genetics , Haemosporida/classification , Haemosporida/genetics , Phylogeny , Protozoan Infections/parasitology , Songbirds/parasitology , Animals , Genetic Speciation , Haplotypes , Host Specificity , Host-Parasite Interactions/genetics , Protozoan Infections/transmission
11.
PLoS One ; 15(8): e0233627, 2020.
Article in English | MEDLINE | ID: mdl-32804928

ABSTRACT

We studied avian development in 49 to 153 species of temperate and tropical New World passerine birds to determine how growth rates, and incubation and nestling periods, varied in relation to other life-history traits. We collected growth data and generated unbiased mass and tarsus growth rate estimates (mass n = 92 species, tarsus n = 49 species), and measured incubation period (n = 151) and nestling period (n = 153), which we analyzed with respect to region, egg mass, adult mass, clutch size, parental care type, nest type, daily nest predation rate (DMR), and nest height. We investigated covariation of life-history and natural-history attributes with the four development traits after controlling for phylogeny. Species in our lowland tropical sample grew 20% (incubation period), 25% (mass growth rate), and 26% (tarsus growth rate) more slowly than in our temperate sample. Nestling period did not vary with respect to latitude, which suggests that tropical songbirds fledge in a less well-developed state than temperate species. Suboscine species typically exhibited slower embryonic and post-embryonic growth than oscine passerines regardless of their breeding region. This pattern of slow development in tropical species could reflect phylogenetic effects based on unknown physiological attributes. Time-dependent nest mortality was unrelated to nestling mass growth rate, tarsus growth rate, and incubation period, but was significantly associated with nestling period. This suggests that nest predation, the predominant cause of nest loss in songbirds, does not exert strong selection on physiologically constrained traits, such as embryonic and post-embryonic growth, among our samples of temperate and lowland tropical songbird species. Nestling period, which is evolutionarily more labile than growth rate, was significantly shorter in birds exposed to higher rates of nest loss and nesting at lower heights, among other traits. Differences in life-history variation across latitudes provide insight into how unique ecological characteristics of each region influence physiological processes of passerines, and thus, how they can shape the evolution of life histories. While development traits clearly vary with respect to latitude, trait distributions overlap broadly. Life-history and natural history associations differ for each development trait, which suggests that unique selective pressures or constraints influence the evolution of each trait.


Subject(s)
Songbirds/growth & development , Animals , Biological Evolution , Climate , Clutch Size , Discriminant Analysis , Ecosystem , Female , Life History Traits , Linear Models , Male , Michigan , Models, Biological , Nesting Behavior/physiology , Oregon , Panama , Phylogeny , Predatory Behavior/physiology , Reproduction/physiology , Selection, Genetic , Songbirds/classification , Songbirds/physiology , Species Specificity , Tarsus, Animal/growth & development , Tropical Climate
12.
Front Plant Sci ; 10: 1580, 2019.
Article in English | MEDLINE | ID: mdl-31850045

ABSTRACT

Identifying the environmental factors that shape intraspecific genetic and phenotypic diversity of species can provide insights into the processes that generate and maintain divergence in highly diverse biomes such as the savannas of the Neotropics. Here, we sampled Qualea grandiflora, the most widely distributed tree species in the Cerrado, a large Neotropical savanna. We analyzed genetic variation with microsatellite markers in 23 populations (418 individuals) and phenotypic variation of 10 metamer traits (internode, petiole and corresponding leaf lamina) in 36 populations (744 individuals). To evaluate the role of geography, soil, climate, and wind speed in shaping the divergence of genetic and phenotypic traits among populations, we used Generalized Dissimilarity Modelling. We also used multiple regressions to further investigate the contributions of those environmental factors on leaf trait diversity. We found high genetic diversity, which was geographically structured. Geographic distance was the main factor shaping genetic divergence in Qualea grandiflora, reflecting isolation by distance. Genetic structure was more related to past climatic changes than to the current climate. We also found high metamer trait variation, which seemed largely influenced by precipitation, soil bulk density and wind speed during the period of metamer development. The high degree of metamer trait variation seems to be due to both, phenotypic plasticity and local adaptation to different environmental conditions, and may explain the success of the species in occupying all the Cerrado biome.

13.
Ecol Evol ; 9(23): 13555-13566, 2019 Dec.
Article in English | MEDLINE | ID: mdl-31871666

ABSTRACT

Parental care in birds varies among species and geographic regions. Incubation behavior influences embryonic development rate and varies substantially among species.We studied attendance at the nest by videoing nests or collecting data from the literature for 112 species in north temperate and lowland tropical sites, then associated patterns of incubation on- and off-bouts with species and environmental traits.Songbirds nesting at low elevations incubate their eggs for an average of 74.1% (±12.9 SD, n = 60 species) of the time in temperate regions and 71.0% (±12.2 SD, n = 52 species) in tropical regions during daylight hours, and 84.3% (±8.2 SD) and 85.3% (±6.2 SD), respectively, of each 24-hr cycle.While these attendance percentages do not differ significantly between latitudes, our data also show that lowland tropical songbirds make fewer visits to the nest and, consequently, have longer on-bouts and off-bouts during incubation. This pattern in attendance reflects a latitudinal contrast in parental care strategy, where lowland tropical birds reduce visits to the nest by increasing on- and off-bout lengths while maintaining the same proportion of time spent incubating their eggs (constancy).Similar constancy across latitude suggests that tropical and temperate birds may be similarly constrained to maintain elevated egg temperatures for normal embryo growth.The different attendance strategies adopted in each region may reflect differences in ambient temperature, adult foraging time, and nest predation rate. Consistently warm ambient temperatures likely allow tropical birds to take longer off-bouts, and thereby to reduce activity around the nest, compared to temperate birds.

14.
PeerJ ; 7: e8013, 2019.
Article in English | MEDLINE | ID: mdl-31720122

ABSTRACT

Evolutionary genomics has recently entered a new era in the study of host-pathogen interactions. A variety of novel genomic techniques has transformed the identification, detection and classification of both hosts and pathogens, allowing a greater resolution that helps decipher their underlying dynamics and provides novel insights into their environmental context. Nevertheless, many challenges to a general understanding of host-pathogen interactions remain, in particular in the synthesis and integration of concepts and findings across a variety of systems and different spatiotemporal and ecological scales. In this perspective we aim to highlight some of the commonalities and complexities across diverse studies of host-pathogen interactions, with a focus on ecological, spatiotemporal variation, and the choice of genomic methods used. We performed a quantitative review of recent literature to investigate links, patterns and potential tradeoffs between the complexity of genomic, ecological and spatiotemporal scales undertaken in individual host-pathogen studies. We found that the majority of studies used whole genome resolution to address their research objectives across a broad range of ecological scales, especially when focusing on the pathogen side of the interaction. Nevertheless, genomic studies conducted in a complex spatiotemporal context are currently rare in the literature. Because processes of host-pathogen interactions can be understood at multiple scales, from molecular-, cellular-, and physiological-scales to the levels of populations and ecosystems, we conclude that a major obstacle for synthesis across diverse host-pathogen systems is that data are collected on widely diverging scales with different degrees of resolution. This disparity not only hampers effective infrastructural organization of the data but also data granularity and accessibility. Comprehensive metadata deposited in association with genomic data in easily accessible databases will allow greater inference across systems in the future, especially when combined with open data standards and practices. The standardization and comparability of such data will facilitate early detection of emerging infectious diseases as well as studies of the impact of anthropogenic stressors, such as climate change, on disease dynamics in humans and wildlife.

15.
Parasitology ; 146(2): 213-219, 2019 02.
Article in English | MEDLINE | ID: mdl-30009719

ABSTRACT

The biogeographic histories of parasites and pathogens are infrequently compared with those of free-living species, including their hosts. Documenting the frequency with which parasites and pathogens disperse across geographic regions contributes to understanding not only their evolution, but also the likelihood that they may become emerging infectious diseases. Haemosporidian parasites of birds (parasite genera Plasmodium, Haemoproteus and Leucocytozoon) are globally distributed, dipteran-vectored parasites. To date, over 2000 avian haemosporidian lineages have been designated by molecular barcoding methods. To achieve their current distributions, some lineages must have dispersed long distances, often over water. Here we quantify such events using the global avian haemosporidian database MalAvi and additional records primarily from the Americas. We scored lineages as belonging to one or more global biogeographic regions based on infection records. Most lineages were restricted to a single region but some were globally distributed. We also used part of the cytochrome b gene to create genus-level parasite phylogenies and scored well-supported nodes as having descendant lineages in regional sympatry or allopatry. Descendant sister lineages of Plasmodium, Haemoproteus and Leucocytozoon were distributed in allopatry in 11, 16 and 15% of investigated nodes, respectively. Although a small but significant fraction of the molecular variance in cytochrome b of all three genera could be explained by biogeographic region, global parasite dispersal likely contributed to the majority of the unexplained variance. Our results suggest that avian haemosporidian parasites have faced few geographic barriers to dispersal over their evolutionary history.


Subject(s)
Bird Diseases/epidemiology , Communicable Diseases, Emerging/epidemiology , Global Health , Haemosporida/physiology , Protozoan Infections, Animal/epidemiology , Analysis of Variance , Animal Migration , Animals , Bird Diseases/parasitology , Bird Diseases/transmission , Birds , Communicable Diseases, Emerging/parasitology , Communicable Diseases, Emerging/transmission , Communicable Diseases, Emerging/veterinary , DNA Barcoding, Taxonomic/veterinary , Diptera/classification , Diptera/parasitology , Genetic Variation , Haemosporida/classification , Insect Vectors/classification , Insect Vectors/parasitology , Likelihood Functions , Phylogeny , Phylogeography , Protozoan Infections, Animal/parasitology , Protozoan Infections, Animal/transmission
16.
Parasitol Res ; 118(1): 191-201, 2019 Jan.
Article in English | MEDLINE | ID: mdl-30536121

ABSTRACT

Accurate detection and identification are essential components for epidemiological, ecological, and evolutionary surveys of avian haemosporidian parasites. Microscopy has been used for more than 100 years to detect and identify these parasites; however, this technique requires considerable training and high-level expertise. Several PCR methods with highly sensitive and specific detection capabilities have now been developed in addition to microscopic examination. However, recent studies have shown that these molecular protocols are insufficient at detecting mixed infections of different haemosporidian parasite species and genetic lineages. In this study, we developed a simple, sensitive, and specific multiplex PCR assay for simultaneous detection and discrimination of parasites of the genera Plasmodium, Haemoproteus, and Leucocytozoon in single and mixed infections. Relative quantification of parasite DNA using qPCR showed that the multiplex PCR can amplify parasite DNA ranging in concentration over several orders of magnitude. The detection specificity and sensitivity of this new multiplex PCR assay were also tested in two different laboratories using previously screened natural single and mixed infections. These findings show that the multiplex PCR designed here is highly effective at identifying both single and mixed infections from all three genera of avian haemosporidian parasites. We predict that this one-step multiplex PCR assay, being convenient and inexpensive, will become a widely used method for molecular screening of avian haemosporidian parasites.


Subject(s)
Bird Diseases/parasitology , Haemosporida/isolation & purification , Multiplex Polymerase Chain Reaction/methods , Plasmodium/isolation & purification , Protozoan Infections, Animal/parasitology , Animals , Bird Diseases/diagnosis , Birds , DNA, Protozoan/genetics , Haemosporida/classification , Haemosporida/genetics , Plasmodium/classification , Plasmodium/genetics , Protozoan Infections, Animal/diagnosis
17.
Mol Ecol ; 27(21): 4336-4346, 2018 11.
Article in English | MEDLINE | ID: mdl-30176078

ABSTRACT

Parasites that can infect multiple host species are considered to be host generalists with low host specificity. However, whether generalist parasites are better adapted to a subset of their host species remains unknown. To elucidate this possibility, we compared the variation in prevalence and infection intensity among host species of three generalist parasite lineages belonging to the morphological species Haemoproteus majoris, in a natural bird community in southern Sweden. Prevalence in each host species was confirmed by nested PCR and DNA sequencing, and infection intensities were quantified using lineage-specific real-time qPCR. For two of the three lineages, we detected positive correlations between prevalence and infection intensity, indicating that these generalist parasites are better adapted to a subset of host species, which may have been more frequently encountered during the evolution of the parasite; we refer to these as main host species. For both lineages, the main host species were more phylogenetically related than expected by chance as revealed by strong phylogenetic signal in prevalence among hosts. By comparing our results with previous records of these parasites, we found that the host range of a generalist parasite can vary among different communities and may partly be shaped by the presence of other parasites. Our study reveals that generalist parasites may be specialized on a subset of their host species and it highlights the importance of considering infection intensity and host phylogeny when determining the host specificity of a parasite.


Subject(s)
Birds/parasitology , Haemosporida/genetics , Host Specificity , Adaptation, Physiological/genetics , Animals , Bird Diseases/parasitology , Genetics, Population , Phylogeny , Sweden
18.
Int J Parasitol ; 48(12): 897-902, 2018 10.
Article in English | MEDLINE | ID: mdl-30076910

ABSTRACT

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.


Subject(s)
Birds/parasitology , Haemosporida/classification , Haemosporida/physiology , Host Specificity , Phylogeny , Animals , Data Mining , Databases, Factual , Databases, Genetic , Haemosporida/genetics , Haemosporida/isolation & purification
19.
PLoS One ; 12(6): e0178791, 2017.
Article in English | MEDLINE | ID: mdl-28575046

ABSTRACT

Habitat modification may change vertebrate and vector-borne disease distributions. However, natural forest regeneration through secondary succession may mitigate these effects. Here we tested the hypothesis that secondary succession influences the distribution of birds and their haemosporidian parasites (genera Plasmodium and Haemoproteus) in a seasonally dry tropical forest, a globally threatened ecosystem, in Brazil. Moreover, we assessed seasonal fluctuations in parasite prevalence and distribution. We sampled birds in four different successional stages at the peak and end of the rainy season, as well as in the middle and at the end of the dry season. A non-metric multidimensional scaling analysis revealed that bird communities in the pasture (i.e., highly modified) areas were different from those in the early, intermediate, and late successional areas (secondary forests). Among 461 individual birds, haemosporidian prevalence was higher in pasture areas than in the more advanced successional stages, but parasite communities were homogeneous across these areas. Parasite prevalence was higher in pasture-specialists birds (resilient species) than in forest-specialists species, suggesting that pasture-specialists may increase infection risk for co-occurring hosts. We found an increase in prevalence between the middle and end of the dry season, a period associated with the beginning of the breeding season (early spring) in southeastern Brazil. We also found effects of seasonality in the relative prevalence of specific parasite lineages. Our results show that natural forest recovery through secondary succession in SDTFs is associated with compositional differences in avian communities, and that advanced successional stages are associated with lower prevalence of avian haemosporidian parasites.


Subject(s)
Birds/parasitology , Ecosystem , Haemosporida/parasitology , Host-Parasite Interactions , Seasons , Animals , Brazil
20.
Parasitology ; 144(7): 984-993, 2017 Jun.
Article in English | MEDLINE | ID: mdl-28290270

ABSTRACT

Parasites of the genera Plasmodium and Haemoproteus (Apicomplexa: Haemosporida) are a diverse group of pathogens that infect birds nearly worldwide. Despite their ubiquity, the ecological and evolutionary factors that shape the diversity and distribution of these protozoan parasites among avian communities and geographic regions are poorly understood. Based on a survey throughout the Neotropics of the haemosporidian parasites infecting manakins (Pipridae), a family of Passerine birds endemic to this region, we asked whether host relatedness, ecological similarity and geographic proximity structure parasite turnover between manakin species and local manakin assemblages. We used molecular methods to screen 1343 individuals of 30 manakin species for the presence of parasites. We found no significant correlations between manakin parasite lineage turnover and both manakin species turnover and geographic distance. Climate differences, species turnover in the larger bird community and parasite lineage turnover in non-manakin hosts did not correlate with manakin parasite lineage turnover. We also found no evidence that manakin parasite lineage turnover among host species correlates with range overlap and genetic divergence among hosts. Our analyses indicate that host switching (turnover among host species) and dispersal (turnover among locations) of haemosporidian parasites in manakins are not constrained at this scale.


Subject(s)
Bird Diseases/epidemiology , Haemosporida/physiology , Host-Parasite Interactions , Malaria/veterinary , Passeriformes , Protozoan Infections, Animal/epidemiology , Animals , Bird Diseases/parasitology , Cytochromes b/genetics , Haemosporida/genetics , Malaria/epidemiology , Malaria/parasitology , Panama/epidemiology , Phylogeny , Plasmodium/genetics , Plasmodium/physiology , Prevalence , Protozoan Infections, Animal/parasitology , Protozoan Proteins/genetics , South America/epidemiology
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