PLOS NEGLECTED TROPICAL DISEASES (2020)

Human Plasmodium vivax diversity, population structure and evolutionary origin

Plasmodium vivax

Abstract

More than 200 million malaria clinical cases are reported each year due to Plasmodium vivax, the most widespread Plasmodium species in the world. This species has been neglected and understudied for a long time, due to its lower mortality in comparison with Plasmodium falciparum. A renewed interest has emerged in the past decade with the discovery of antimalarial drug resistance and of severe and even fatal human cases. Nonetheless, today there are still significant gaps in our understanding of the population genetics and evolutionary history of P. vivax, particularly because of a lack of genetic data from Africa. To address these gaps, we genotyped 14 microsatellite loci in 834 samples obtained from 28 locations in 20 countries from around the world. We discuss the worldwide population genetic structure and diversity and the evolutionary origin of P. vivax in the world and its introduction into the Americas. This study demonstrates the importance of conducting genome-wide analyses of P. vivax in order to unravel its complex evolutionary history.

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diagram - research evolution adaptation plasmodium vivax-like african great apes humans - virginie rougeron

diagram - research evolution adaptation plasmodium vivax-like african great apes chacma baboon virginie rougeron

Fig. 1 Worldwide samples distribution per country. For each country are indicated the number of samples collected (N) and the number of mono-infected samples (Nm). In yellow are represented Asian countries, in purple the Middle-east countries, in grey African countries and in green American countries. Map adapted from Malaria Atlas Project (MAP), University of Oxford.

Fig. 2 Overall allelic richness, Hs and rDbar were estimated using all loci for each population. A. Allelic richness for each continent. B. Hs for each continent. C. rDbar for each continent. Allelic richness, Hs and rDbar were estimated overall loci for each population. Boxes represent the interquartile range between first and third quartiles and the line inside represents the median of the estimate per population. Points represent outliers beyond the whiskers. The different regions of the world are represented using different colors: South East Asia (in yellow), the Middle East (in purple), Africa (in grey) and America (in green).

Fig. 3 Worldwide genetic structure of 575 P. vivax isolates collected around the world. A. Neighbor-joining tree of isolates based on Cavalli-Sforza distance, with bootstrap resampling (N = 500); Red and orange dots indicate the bootstrap values, ranging from 0.9 to 1, and from 0.6 to 0.89 respectively. B. MultiDimensional Scaling representation. AFR: Central African Republic + Cameroon + Togo; ARM: Armenia; AZE: Azerbaijan; BAN: Bandarban; BAY: Bay Islands; CAM: Camopi; CAY: Cayenne; COX: Cox’s Bazar; ETH: Ethiopia; HLF: New Halfa; HND: Honduras; IND: India; IRN: Iran; KGR: Khagrachari; KHA: Khartoum; MEX: Mexico; MRT: Mauritania; PAK: Pakistan; PER: Peru; STG: Saint Georges de l’Oyapock; THA: Thailand; TMY: Thailand/Myanmar; TUR: Turkey; VEN: Venezuela. In yellow are represented Asian countries, in purple Middle-east countries, in grey African countries and in green American countries.

Fig. 4 Bayesian cluster analysis on 575 P. vivax isolates collected around the world, using STRUCTURE software, for K = 2, K = 4 and K = 6. Map adapted from Malaria Atlas Project (MAP), University of Oxford. AFR: Central African Republic + Cameroon + Togo; ARM: Armenia; AZE: Azerbaijan; BAN: Bandarban; BAY: Bay Islands; CAM: Camopi; CAY: Cayenne; COX: Cox’s Bazar; ETH: Ethiopia; HLF: New Halfa; HND: Honduras; IND: India; IRN: Iran; KGR: Khagrachari; KHA: Khartoum; MEX: Mexico; MRT: Mauritania; PAK: Pakistan; PER: Peru; STG: Saint Gorges de l’Oyapock; THA: Thailand; TMY: Thailand/Myanmar; TUR: Turkey; VEN: Venezuela. In yellow are represented Asian countries, in purple Middle-east countries, in grey African countries and in green American countries.

Publication infos

Authors Virginie Rougeron, Eric Elguero, Celine Arnathau, Beatriz Acuña Hidalgo, Patrick Durand, Sandrine Houze, Antoine Berry, Sedigheh Zakeri, Rashidul Haque, Mohammad Shafiul Alam, Francois Nosten, Carlo Severini, Tamirat Gebru Woldearegai, Benjamin Mordmuller, Peter Gottfried Kremsner, Lilia Gonzalez-Ceron, Gustavo Fontecha, Dionicia Gamboa, Lise Musset, Eric Legrand, Oscar Noya, Tepanata Pumpaibool, Pingchai Harnyuttanakorn, Khadijetou Mint Lekweiry, Musab Mohamad Albsheer, Muzamil Mahdi Abdel Hamid, Ali Ould Mohamed Salem Boukary, Jean-Francois Trape, Francois Renaud, Franck Prugnolle
Corresponding authors emails virginie.rougeron@cnrs.fr; rougeron.virginie@gmail.com
Affilitions Laboratoire MIVEGEC (Universite de Montpellier-CNRS-IRD) - CREES, Montpellier, France - Service de Parasitologie-mycologie CNR du Paludisme, AP-HP Hopital Bichat, Paris, France - Centre de Physiopathologie de Toulouse-Purpan (CPTP), Institut National de la Sante et de la Recherche Medicale (INSERM) UMR1043, CNRS UMR5282, Universite de Toulouse Paul Sabatier, F-31300 Toulouse, France - Service de Parasitologie-Mycologie, Institut Federatif de Biologie, Centre Hospitalier Universitaire de Toulouse, F-31300 Toulouse, France - Malaria and Vector Research Group (MVRG), Biotechnology Research Center (BRC), Pasteur Institute of Iran, Tehran, Iran - Emerging Infections & Parasitology Laboratory, icddr,b, Mohakhali, Dhaka, Bangladesh - Centre for Tropical Medicine and Global Health, Oxford, United Kingdom - Shoklo Malaria Research Unit, Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, Mae Sot, Thailand - Department of Infectious Diseases, Istituto Superiore di Sanità, Rome, Italy - Institute of Tropical Medicine, University of Tubingen, Tubingen, Germany - German Centre for Infection Research (DZIF), partner site Tubingen, Tubingen, Germany - Department of Medical Laboratory Sciences, College of Medical and Health Sciences, Haramaya University, Harar, Ethiopia - Regional Centre of Research in Public Health, National Institute of Public Health, Tapachula, Chiapas, Mexico - Microbiology Research Institute, Universidad Nacional Autonoma de Honduras, Tegucigalpa, Honduras - Instituto de Medicina Tropical Alexander Von Humboldt, Universidad Peruana Cayetano Heredia, AP, Lima, Peru - Unit, Institut Pasteur de Guyane, BP6010, French Guiana - Malaria Genetic and Resistance Group, Biology of Host-Parasite Interactions Unit, Institut Pasteur, Paris, France - Centro para Estudios Sobre Malaria, Instituto de Altos Estudios en Salud Dr. Arnoldo Gabaldo, Ministerio del Poder Popular para la Salud and Instituto de Medicina Tropical, Universidad Central de Venezuela, Maracay, Caracas, Venezuela - Biomedical Science, Graduate School, Chulalongkorn University, Bangkok, Thailand - Malaria Research Programme, College of Public Health Science, Chulalongkorn University, Bangkok, Thailand - Department of Biology, Faculty of Science, Chulalongkorn University, Bangkok,Thailand - UR-Genomes et milieux, Faculte des Sciences et Techniques, Nouakchott Al-Aasriya, Mauritania - Department of Parasitology and Medical Entomology, Medical Campus, University of Khartoum, Sudan - Aix Marseille Univ, IRD, AP-HM, SSA, VITROME, Marseille, France
Fundings Authors thank the ANR Tremplin EVAD 2017, IRD and CNRS-INEE. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.