Thaís C de Oliveira1, Priscila T Rodrigues1, Angela M Early2,3, Ana Maria R C Duarte4,5, Julyana C Buery6, Marina G Bueno7,8, José L Catão-Dias7, Crispim Cerutti6, Luísa D P Rona9,10, Daniel E Neafsey2,3, Marcelo U Ferreira1. 1. Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil. 2. Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA. 3. Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, USA. 4. Laboratory of Biochemistry and Molecular Biology, Superintendency for the Control of Endemics (SUCEN), State Secretary of Health, São Paulo, Brazil. 5. Laboratory of Protozoology, Institute of Tropical Medicine of São Paulo, University of São Paulo, São Paulo, Brazil. 6. Department of Social Medicine, Center for Health Sciences, Federal University of Espírito Santo, Vitória, Brazil. 7. Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, Brazil. 8. Laboratory of Comparative and Environmental Virology, Oswaldo Cruz Institute, Fiocruz, Rio de Janeiro, Brazil. 9. Department of Cell Biology, Embryology, and Genetics, Federal University of Santa Catarina, Florianópolis, Brazil. 10. National Council for Scientific and Technological Development, National Institute of Science and Technology in Molecular Entomology, Rio de Janeiro, Brazil.
Abstract
BACKGROUND: The population history of Plasmodium simium, which causes malaria in sylvatic Neotropical monkeys and humans along the Atlantic Coast of Brazil, remains disputed. Genetically diverse P vivax populations from various sources, including the lineages that founded the species P simium, are thought to have arrived in the Americas in separate migratory waves. METHODS: We use population genomic approaches to investigate the origin and evolution of P simium. RESULTS: We find a minimal genome-level differentiation between P simium and present-day New World P vivax isolates, consistent with their common geographic origin and subsequent divergence on this continent. The meagre genetic diversity in P simium samples from humans and monkeys implies a recent transfer from humans to non-human primates - a unique example of malaria as a reverse zoonosis of public health significance. Likely genomic signatures of P simium adaptation to new hosts include the deletion of >40% of a key erythrocyte invasion ligand, PvRBP2a, which may have favored more efficient simian host cell infection. CONCLUSIONS: New World P vivax lineages that switched from humans to platyrrhine monkeys founded the P simium population that infects nonhuman primates and feeds sustained human malaria transmission in the outskirts of major cities.
BACKGROUND: The population history of Plasmodium simium, which causes malaria in sylvatic Neotropical monkeys and humans along the Atlantic Coast of Brazil, remains disputed. Genetically diverse P vivax populations from various sources, including the lineages that founded the species P simium, are thought to have arrived in the Americas in separate migratory waves. METHODS: We use population genomic approaches to investigate the origin and evolution of P simium. RESULTS: We find a minimal genome-level differentiation between P simium and present-day New World P vivax isolates, consistent with their common geographic origin and subsequent divergence on this continent. The meagre genetic diversity in P simium samples from humans and monkeys implies a recent transfer from humans to non-human primates - a unique example of malaria as a reverse zoonosis of public health significance. Likely genomic signatures of P simium adaptation to new hosts include the deletion of >40% of a key erythrocyte invasion ligand, PvRBP2a, which may have favored more efficient simian host cell infection. CONCLUSIONS: New World P vivax lineages that switched from humans to platyrrhine monkeys founded the P simium population that infects nonhuman primates and feeds sustained human malaria transmission in the outskirts of major cities.
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