Genomic analysis of a pre-elimination Malaysian Plasmodium vivax population reveals selective pressures and changing transmission dynamics

Auburn, Sarah; Benavente, Ernest Diez; Miotto, Olivo; Pearson, Richard D.; Amato, Roberto; Grigg, Matthew J.; Barber, Bridget E.; William, Timothy; Handayuni, Irene; Marfurt, Jutta; Trimarsanto, Hidayat; Noviyanti, Rintis; Sriprawat, Kanlaya; Nosten, François; Campino, Susana; Clark, Taane G.; Anstey, Nicholas M.; Kwiatkowski, Dominic P.; Price, Ric N.

doi:10.1038/s41467-018-04965-4

Cited by 71 publications

(107 citation statements)

References 65 publications

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“…Recently, technological improvement has made possible to sequence the whole P. vivax genome via an enrichment of the parasite DNA from clinical blood samples ( 11 ). This methodological breakthrough marked the beginning of a new era in the field, with the released in a few years of several projects characterizing the pathogen genetic variation at the whole genome scale in several P. vivax populations ( 12–15 ). Those projects shed light on strong signals of recent evolutionary selection partly due to known drug resistance genes.…”

Section: Introductionmentioning

confidence: 99%

Population genomic evidence of a Southeast Asian origin ofPlasmodium vivax

Daron

Boissière

Ngoubangoye

et al. 2020

Preprint

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20Plasmodium vivax is the most prevalent and widespread human malaria parasite, 21 with almost three billion people living at risk of infection. With the discovery of its closest 22 genetic relatives in African great apes (Plasmodium vivax-like), the origin of P. vivax has 23 been proposed to be located in the sub-Saharan African area. However, the limited number 24 of genetic markers and samples investigated questioned the robustness of this result. Here, 25 we examined the population genomic variation of 447 human P. vivax strains and 19 ape P. 26 vivax-like strains originating from 24 different countries across the world. We identified 27 2,005,455 high quality single-nucleotide polymorphism loci allowing us to conduct an 28 extensive characterization to date of P. vivax worldwide genetic variation. Phylogenetic 29 relationships between human and ape Plasmodium revealed that P. vivax is a sister clade of 30 P. vivax-like, not included within the radiation of P. vivax-like. By investigating a variety of 31 aspects of P. vivax variation, we identified several striking geographical patterns in summary 32 statistics as function of increasing geographic distance from Southeast Asia, suggesting that 33 P. vivax may derived from serial founder effects from a single origin located in Asia. 34 evolutionary selection partly due to known drug resistance genes. However, even though 62 they released hundreds of complete genomes, each of them restricted their investigation on 63 a sub-fraction of the worldwide P. vivax diversity, either located in Asia-Pacific or South 64America. Consequently, a comprehensive picture of the worldwide genetic diversity and 65 structure of P. vivax populations is still missing and its evolutionary history and how it spread 66 over the world is still poorly understood. Moreover, despite growing evidence suggesting an 67 underlying widespread presence of P. vivax across all malaria-endemic regions of Africa from this area. Thus, a key challenge is to provide a worldwide understanding of the genetic 70 variability of P. vivax at the genome level to bring insights on the past demographic history 71 and origin of this pathogen. 72The origin of current P. vivax in humans has stimulated passionate and exciting 73 debates for years. Certain studies placed the origin of the human P. vivax in Southeast Asia 74 ("out of Asia" hypothesis) based on its phylogenetic position in a clade of parasites infecting 75Asian monkeys (17)(18)(19). This scenario was also supported by genotyping data at 11 76 microsatellite markers collected across four continents, showing the highest microsatellite 77 diversity in Southeast Asia (20, 21). However, the Asian-origin has been challenged by an 78 "out of Africa" scenario, with the recent discovery of a closely related Plasmodium species 79 circulating in wild-living African great apes (chimpanzees and gorillas) (22). This new 80 lineage, hereafter referred to as P. vivax-like, was suggested to have given rise to P. vivax in 81 humans following the transfer of parasit...

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Section: Introductionmentioning

confidence: 99%

Population genomic evidence of a Southeast Asian origin ofPlasmodium vivax

Daron

Boissière

Ngoubangoye

et al. 2020

Preprint

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“…Measures of relatedness used in studies of malaria include those estimated under HMMs (hmmIBD [18], used in e.g. [19,20,21,22]; isoRelate [23], extension of XIBD [24]; DEploidIBD [25], extension of DEploid [26]). Measures based on IBS (e.g.…”

Section: Introductionmentioning

confidence: 99%

Estimating relatedness between malaria parasites

Taylor

Jacob

Neafsey

et al. 2019

Preprint

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Understanding the relatedness of individuals within or between populations is a common goal in biology. Increasingly, relatedness features in genetic epidemiology studies of pathogens. These studies are relatively new compared to those in humans and other organisms, but are important for designing interventions and understanding pathogen transmission. Only recently have researchers begun to routinely apply relatedness to apicomplexan eukaryotic malaria parasites, and to date have used a range of different approaches on an ad hoc basis. It remains unclear how to compare different studies, therefore, and which measures to use. Here, we systematically compare measures based on identity-by-state and identity-by-descent using a globally diverse data set of malaria parasites, Plasmodium falciparum and Plasmodium vivax, and provide marker requirements for estimates based on identity-by-descent. We formally show that the informativeness of polyallelic markers for relatedness inference is maximised when alleles are equifrequent. Estimates based on identity-bystate are sensitive to allele frequencies, which vary across populations and by experimental design. For portability across studies, we thus recommend estimates based on identity-by-descent. To generate reliable estimates, we recommend approximately 200 biallelic or 100 polyallelic markers. Confidence intervals illuminate inference across studies based on different sets of markers. These marker requirements, unlike many thus far reported, are immediately applicable to haploid malaria parasites and other haploid eukaryotes. This is the first attempt to provide rigorous analysis of the reliability of, and requirements for, relatedness inference in malaria genetic epidemiology, and will provide a basis for statistically informed prospective study design and surveillance strategies.

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“…The analysis included genomic data on P. vivax isolates collected from 26 countries. Published data were included from 19 countries derived from the European Nucleotide Archive 11–15 , and new data from 10 countries (Supplementary Table 1, Supplementary Figure 1). New genomic data were derived from patients recruited to partner studies in Afghanistan, Bangladesh, Bhutan, Colombia, Ethiopia, Indonesia, Iran, Malaysia, Sudan, and Vietnam.…”

Section: Methodsmentioning

confidence: 99%

“…New genomic data were derived from patients recruited to partner studies in Afghanistan, Bangladesh, Bhutan, Colombia, Ethiopia, Indonesia, Iran, Malaysia, Sudan, and Vietnam. With the exception of Colombia, the patient sampling frameworks have been described previously 11,12,14,16–20 . The samples from Colombia were collected within the framework of cross-sectional epidemiological surveys conducted between 2013 and 2017.…”

Section: Methodsmentioning

confidence: 99%

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A molecular barcode and online tool to identify and map imported infection with Plasmodium vivax

Trimarsanto

Amato

Pearson

et al. 2019

Preprint

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Imported cases present a considerable challenge to the elimination of malaria. Traditionally, patient travel history has been used to identify imported cases, but the long-latency liver stages confound this approach in Plasmodium vivax. Molecular tools to identify and map imported cases offer a more robust approach, that can be combined with drug resistance and other surveillance markers in high-throughput, population-based genotyping frameworks. Using a machine learning approach incorporating hierarchical FST (HFST) and decision tree (DT) analysis applied to 831 P. vivax genomes from 20 countries, we identified a 28-Single Nucleotide Polymorphism (SNP) barcode with high capacity to predict the country of origin. The Matthews correlation coefficient (MCC), which provides a measure of the quality of the classifications, ranging from −1 (total disagreement) to 1 (perfect prediction), exceeded 0.9 in 15 countries in cross-validation evaluations. When combined with an existing 37-SNP P. vivax barcode, the 65-SNP panel exhibits MCC scores exceeding 0.9 in 17 countries with up to 30% missing data. As a secondary objective, several genes were identified with moderate MCC scores (median MCC range from 0.54-0.68), amenable as markers for rapid testing using low-throughput genotyping approaches. A likelihood-based classifier framework was established, that supports analysis of missing data and polyclonal infections. To facilitate investigator-lead analyses, the likelihood framework is provided as a web-based, open-access platform (vivaxGEN-geo) to support the analysis and interpretation of data produced either at the 28-SNP core or full 65-SNP barcode. These tools can be used by malaria control programs to identify the main reservoirs of infection so that resources can be focused to where they are needed most.

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Genomic analysis of a pre-elimination Malaysian Plasmodium vivax population reveals selective pressures and changing transmission dynamics

Cited by 71 publications

References 65 publications

Population genomic evidence of a Southeast Asian origin ofPlasmodium vivax

Population genomic evidence of a Southeast Asian origin ofPlasmodium vivax

Estimating relatedness between malaria parasites

A molecular barcode and online tool to identify and map imported infection with Plasmodium vivax

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