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      Population Genetics of the Filarial Worm Wuchereria bancrofti in a Post-treatment Region of Papua New Guinea: Insights into Diversity and Life History

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          Wuchereria bancrofti (Wb) is the primary causative agent of lymphatic filariasis (LF). Our studies of LF in Papua New Guinea (PNG) have shown that it is possible to reduce the prevalence of Wb in humans and mosquitoes through mass drug administration (MDA; diethylcarbamazine with/without ivermectin). While MDAs in the Dreikikir region through 1998 significantly reduced prevalence of Wb infection, parasites continue to be transmitted in the area.


          We sequenced the Wb mitochondrial Cytochrome Oxidase 1 (CO1) gene from 16 people infected with Wb. Patients were selected from 7 villages encompassing both high and moderate annual transmission potentials (ATP). We collected genetic data with the objectives to (i) document contemporary levels of genetic diversity and (ii) distinguish between populations of parasites and hosts across the study area.

          Principle Findings

          We discovered 109 unique haplotypes currently segregating in the Wb parasite population, with one common haplotype present in 15 out of 16 infections. We found that parasite diversity was similar among people residing within the same village and clustered within transmission zones. For example, in the high transmission area, diversity tended to be more similar between neighboring villages, while in the moderate transmission area, diversity tended to be less similar.


          In the Dreikikir region of PNG there are currently high levels of genetic diversity in populations of Wb. High levels of genetic diversity may complicate future MDAs in this region and the presence of dominant haplotypes will require adjustments to current elimination strategies.

          Author Summary

          The Global Program to Eliminate Lymphatic Filariasis (LF), initiated by the World Health Organization (WHO), aims to eliminate LF from endemic regions, where 1.34 billion people live at risk of this disease. The causative agent responsible for 90% of LF is the nematode parasite species Wuchereria bancrofti (Wb). The primary approach to LF elimination has been through mass drug administration (MDA), which serves to interrupt transmission by killing the microfilaria required to continue the parasite life cycle through mosquito transmission. Despite success of MDA, evidence indicates that transmission can rebound if drug administration is discontinued. In the void of well-characterized genetic markers, it is difficult to understand how a Wb population will be impacted by or recover from MDA. Here we use recently described mitochondrial DNA polymorphisms to evaluate the diversity of a Wb population that has been previously exposed to MDA in Papua New Guinea. Our data analyses reveal significant genetic diversity and evidence that MDA has not significantly reduced the genetic complexity of the Wb population. This study describes a population genetic approach for assessing the impact of MDA and other transmission control strategies.

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          Most cited references 37

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          Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.

          We present here a new version of the Arlequin program available under three different forms: a Windows graphical version (Winarl35), a console version of Arlequin (arlecore), and a specific console version to compute summary statistics (arlsumstat). The command-line versions run under both Linux and Windows. The main innovations of the new version include enhanced outputs in XML format, the possibility to embed graphics displaying computation results directly into output files, and the implementation of a new method to detect loci under selection from genome scans. Command-line versions are designed to handle large series of files, and arlsumstat can be used to generate summary statistics from simulated data sets within an Approximate Bayesian Computation framework. © 2010 Blackwell Publishing Ltd.
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            UCHIME improves sensitivity and speed of chimera detection

            Motivation: Chimeric DNA sequences often form during polymerase chain reaction amplification, especially when sequencing single regions (e.g. 16S rRNA or fungal Internal Transcribed Spacer) to assess diversity or compare populations. Undetected chimeras may be misinterpreted as novel species, causing inflated estimates of diversity and spurious inferences of differences between populations. Detection and removal of chimeras is therefore of critical importance in such experiments. Results: We describe UCHIME, a new program that detects chimeric sequences with two or more segments. UCHIME either uses a database of chimera-free sequences or detects chimeras de novo by exploiting abundance data. UCHIME has better sensitivity than ChimeraSlayer (previously the most sensitive database method), especially with short, noisy sequences. In testing on artificial bacterial communities with known composition, UCHIME de novo sensitivity is shown to be comparable to Perseus. UCHIME is >100× faster than Perseus and >1000× faster than ChimeraSlayer. Contact: Availability: Source, binaries and data: Supplementary information: Supplementary data are available at Bioinformatics online.
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              Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.

               F Tajima (1989)
              The relationship between the two estimates of genetic variation at the DNA level, namely the number of segregating sites and the average number of nucleotide differences estimated from pairwise comparison, is investigated. It is found that the correlation between these two estimates is large when the sample size is small, and decreases slowly as the sample size increases. Using the relationship obtained, a statistical method for testing the neutral mutation hypothesis is developed. This method needs only the data of DNA polymorphism, namely the genetic variation within population at the DNA level. A simple method of computer simulation, that was used in order to obtain the distribution of a new statistic developed, is also presented. Applying this statistical method to the five regions of DNA sequences in Drosophila melanogaster, it is found that large insertion/deletion (greater than 100 bp) is deleterious. It is suggested that the natural selection against large insertion/deletion is so weak that a large amount of variation is maintained in a population.

                Author and article information

                Role: Editor
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, USA )
                July 2013
                11 July 2013
                : 7
                : 7
                [1 ]Center for Global Health and Diseases, Case Western Reserve University, Cleveland, Ohio, United States of America
                [2 ]Papua New Guinea Institute of Medical Research, Goroka, Papua New Guinea
                [3 ]Centre for Neglected Tropical Diseases, Liverpool School of Tropical Medicine, Liverpool, United Kingdom
                University of Melbourne, Australia
                Author notes

                ¶ These authors are first co-authors.

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: STS MJB JWK DJT PAZ. Performed the experiments: STS AR. Analyzed the data: STS AR KB PAZ. Contributed reagents/materials/analysis tools: LR ET MB MJB PS JWK DJT PAZ. Wrote the paper: STS PAZ.


                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Pages: 10
                Financial support for this study was provided through grants from the National Institutes of Health to JWK and PAZ (AI065717) and to DJT (AI097262), the Fogarty International Center to PAZ (TW007872), and a T32 Postdoctoral Fellowship in Geographic Medicine and Infectious Disease to STS (AI007024). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Research Article
                Population Biology
                Global Health
                Infectious Diseases
                Neglected Tropical Diseases
                Parasitic Diseases

                Infectious disease & Microbiology


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