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"Bell, Jeffrey A."
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Parasite Prevalence Corresponds to Host Life History in a Diverse Assemblage of Afrotropical Birds and Haemosporidian Parasites
Avian host life history traits have been hypothesized to predict rates of infection by haemosporidian parasites. Using molecular techniques, we tested this hypothesis for parasites from three haemosporidian genera (Plasmodium, Haemoproteus, and Leucocytozoon) collected from a diverse sampling of birds in northern Malawi. We found that host life history traits were significantly associated with parasitism rates by all three parasite genera. Nest type and nest location predicted infection probability for all three parasite genera, whereas flocking behavior is an important predictor of Plasmodium and Haemoproteus infection and habitat is an important predictor of Leucocytozoon infection. Parasite prevalence was 79.1% across all individuals sampled, higher than that reported for comparable studies from any other region of the world. Parasite diversity was also exceptionally high, with 248 parasite cytochrome b lineages identified from 152 host species. A large proportion of Plasmodium, Haemoproteus, and Leucocytozoon parasite DNA sequences identified in this study represent new, previously undocumented lineages (n = 201; 81% of total identified) based on BLAST queries against the avian malaria database, MalAvi.
Journal Article
Haemosporidian infection risk and community structure determined by duck feeding guild
Birds possess the most diverse assemblage of haemosporidian parasites, although the true diversity is unknown due to high genetic diversity and insufficient sampling across all avian clades. Waterfowl (Order Anseriformes) are an ideal group to discover hidden parasite diversity and examine the role of host ecology in parasite transmission. Waterfowl contain 2 distinct feeding guilds, dabbling and diving, which differ in niche utilization that likely alters vector encounter rates and haemosporidian parasite risk. To determine the role of feeding guild in haemosporidian parasitism we analysed 223 blood samples collected by hunters from the upper Midwest of the United States from 2017 to 2019. Fifty-four individuals were infected by haemosporidian parasites (24·2% prevalence). Infection prevalence differed significantly between dabbling (34·9%, n = 109) and diving (14·0%, n = 114) ducks. Feeding guild was the only host trait that could predict haemosporidian infection risk, with a significantly higher risk in dabbling ducks. Twenty-four haemosporidian lineages were identified, with 9 identified for the first time. Thirteen lineages were found only in dabbling ducks, 5 only in diving ducks and 6 in both feeding guilds. Community analysis showed that each feeding guild harboured a unique parasite community. There was no phylogenetic signal of feeding guild within a phylogenetic reconstruction of North American waterfowl haemosporidian lineages. Our results demonstrate that waterfowl contain a diverse and distinct community of haemosporidian parasites. The unique composition of each feeding guild determines not only haemosporidian infection risk but also community structure. This is the first report of such an impact for waterfowl feeding guilds.
Journal Article
Harnessing free energy calculations for kinome-wide selectivity in drug discovery campaigns with a Wee1 case study
Optimizing both on-target and off-target potencies is essential for developing effective and selective small-molecule therapeutics. Free energy calculations offer rapid potency predictions, usually within hours and with experimental accuracy and thus enables efficient identification of promising compounds for synthesis, accelerating early-stage drug discovery campaigns. While free energy predictions are routinely applied to individual proteins, here, we present a free energy framework for efficiently achieving kinome-wide selectivity that led to the discovery of selective Wee1 kinase inhibitors. Ligand-based relative binding free energy calculations rapidly identified multiple novel potent chemical scaffolds. Subsequent protein residue mutation free energy calculations that modified the Wee1 gatekeeper residue, significantly reduced their off-target liabilities across the kinome. Thus, with judicious use of this gatekeeper residue selectivity handle, applying this computational strategy streamlined the optimization of both on-target and off-target potencies, offering a roadmap to expedite drug discovery timelines by decreasing unanticipated off-target toxicities.
Free energy calculations are an essential tool to identify targets for individual proteins. Here, authors describe free energy perturbation (FEP+) calculations to optimise on target and off-target potencies for the discovery of potent Wee1 inhibitors with kinome-wide selectivity.
Journal Article
Avian malaria, ecological host traits and mosquito abundance in southeastern Amazonia
Avian malaria is a vector transmitted disease caused by Plasmodium and recent studies suggest that variation in its prevalence across avian hosts is correlated with a variety of ecological traits. Here we examine the relationship between prevalence and diversity of Plasmodium lineages in southeastern Amazonia and: (1) host ecological traits (nest location, nest type, flocking behaviour and diet); (2) density and diversity of avian hosts; (3) abundance and diversity of mosquitoes; and (4) season. We used molecular methods to detect Plasmodium in blood samples from 675 individual birds of 120 species. Based on cytochrome b sequences, we recovered 89 lineages of Plasmodium from 136 infected individuals sampled across seven localities. Plasmodium prevalence was homogeneous over time (dry season and flooding season) and space, but heterogeneous among 51 avian host species. Variation in prevalence among bird species was not explained by avian ecological traits, density of avian hosts, or mosquito abundance. However, Plasmodium lineage diversity was positively correlated with mosquito abundance. Interestingly, our results suggest that avian host traits are less important determinants of Plasmodium prevalence and diversity in southeastern Amazonia than in other regions in which they have been investigated.
Journal Article
A new real-time PCR protocol for detection of avian haemosporidians
Background
Birds possess the most diverse assemblage of haemosporidian parasites; including three genera,
Plasmodium
,
Haemoproteus
, and
Leucocytozoon
. Currently there are over 200 morphologically identified avian haemosporidian species, although true species richness is unknown due to great genetic diversity and insufficient sampling in highly diverse regions. Studies aimed at surveying haemosporidian diversity involve collecting and screening samples from hundreds to thousands of individuals. Currently, screening relies on microscopy and/or single or nested standard PCR. Although effective, these methods are time and resource consuming, and in the case of microscopy require substantial expertise. Here we report a newly developed real-time PCR protocol designed to quickly and reliably detect all three genera of avian haemosporidians in a single biochemical reaction.
Methods
Using available DNA sequences from avian haemosporidians we designed primers R330F and R480RL, which flank a 182 base pair fragment of mitochondrial conserved rDNA. These primers were initially tested using real-time PCR on samples from Malawi, Africa, previously screened for avian haemosporidians using traditional nested PCR. Our real time protocol was further tested on 94 samples from the Cerrado biome of Brazil, previously screened using a single PCR assay for haemosporidian parasites. These samples were also amplified using modified nested PCR protocols, allowing for comparisons between the three different screening methods (single PCR, nested PCR, real-time PCR).
Results
The real-time PCR protocol successfully identified all three genera of avian haemosporidians from both single and mixed infections previously detected from Malawi. There was no significant difference between the three different screening protocols used for the 94 samples from the Brazilian Cerrado (
χ
2
= 0.3429, df = 2, P = 0.842). After proving effective, the real-time protocol was used to screen 2113 Brazilian samples, identifying 693 positive samples.
Conclusions
Our real-time PCR assay proved as effective as two widely used molecular screening techniques, single PCR and nested PCR. However, the real-time protocol has the distinct advantage of detecting all three genera in a single reaction, which significantly increases efficiency by greatly decreasing screening time and cost. Our real-time PCR protocol is therefore a valuable tool in the quickly expanding field of avian haemosporidian research.
Journal Article
Between‐ and within‐population drivers of haemosporidian prevalence and diversity in American robins Turdus migratorius
Avian haemosporidians are a diverse group of parasites that infect birds worldwide and have been a major focus of research for decades. Yet, few studies have identified the drivers of infection at the intraspecific host level. We aimed to study the drivers of prevalence and diversity of haemosporidian parasites infecting a common North American songbird species, the American robin Turdus migratorius, which breeds across most of the continent. We found little seasonal variation in haemosporidian prevalence in robins, although we detected a significantly positive relationship between robin breeding latitude and co‐infection with different haemosporidian parasite lineages. Additionally, robins infected with Plasmodium had substantially better body condition than uninfected robins, which could be due to migratory culling. We detected 31 haemosporidian lineages among the robins we sampled, of which eight were novel. When matched against known haemosporidian lineages, our results suggest that robins harbor a higher diversity of haemosporidian parasites than previously known. The results of this study suggest that comparisons of common, widespread bird species such as robins across their range could help unveil novel aspects of the haemosporidian–host relationship and how such a relationship may change under current and future rapid environmental change.
Journal Article
Bird Tissues from Museum Collections are Reliable for Assessing Avian Haemosporidian Diversity
Birds harbor a diverse group of haemosporidian parasites that reproduce and develop in the host blood cells, muscle tissue, and various organs, which can cause negative effects on the survival and reproduction of their avian hosts. Characterization of the diversity, distribution, host specificity, prevalence patterns, and phylogenetic relationships of these parasites is critical to the study of avian host–parasite ecology and evolution and for understanding and preventing epidemics in wild bird populations. Here, we tested whether muscle and liver samples collected as part of standard ornithological museum expeditions can be examined to study the diversity and distributions of haemosporidians in the same way as blood collected from individual birds that are typically banded and released. We used a standard molecular diagnostic screening method for mitochondrial DNA (cytochrome b) of the parasites and found that blood, muscle, and liver collected from the same host individual provide similar estimates of prevalence and diversity of haemosporidians from the genera Parahaemoproteus and Leucocytozoon. Although we found higher prevalence for the genus Plasmodium when we screened blood vs. liver and muscle samples, the estimates of the diversity of Plasmodium from different tissue types are not affected at the community level. Given these results, we conclude that for several reasons existing museum genetic resources collections are valuable data sources for the study of haemosporidians. First, ornithological museum collections around the world house tens of thousands of vouchered tissue samples collected from remote regions of the world. Second, the host specimens are vouchered and thus host identification and phenotype are permanently documented in databased archives with a diversity of associated ancillary data. Thus, not only can identifications be confirmed but also a diversity of morphological measurements and data can be measured and accessed for these host specimens in perpetuity.
Journal Article
Avian malaria and related parasites from resident and migratory birds in the brazilian atlantic forest, with description of a new Haemoproteus species
Determining the prevalence and local transmission dynamics of parasitic organisms are necessary to understand the ability of parasites to persist in host populations and disperse across regions, yet local transmission dynamics, diversity, and distribution of haemosporidian parasites remain poorly understood. We studied the prevalence, diversity, and distributions of avian haemosporidian parasites of the genera Plasmodium, Haemoproteus, and Leucocytozoon among resident and migratory birds in Serra do Mar, Brazil. Using 399 blood samples from 66 Atlantic Forest bird species, we determined the prevalence and molecular diversity of these pathogens across avian host species and described a new species of Haemoproteus. Our molecular and morphological study also revealed that migratory species were infected more than residents. However, vector infective stages (gametocytes) of Leucocytozoon spp., the most prevalent parasites found in the most abundant migrating host species in Serra do Mar (Elaenia albiceps), were not seen in blood films of local birds suggesting that this long-distance Austral migrant can disperse Leucocytozoon parasite lineages from Patagonia to the Atlantic Forest, but lineage sharing among resident species and local transmission cannot occur in this part of Brazil. Our study demonstrates that migratory species may harbor a higher diversity and prevalence of parasites than resident species, but transportation of some parasites by migratory hosts may not always affect local transmission.
Journal Article