Plasmodium simium: Population Genomics Reveals the Origin of a Reverse Zoonosis.
Thaís C de Oliveira, Priscila T Rodrigues, Angela M Early, Ana Maria R C Duarte, Julyana C Buery, Marina G Bueno, José L Catão-Dias, Crispim Cerutti, Luísa D P Rona, Daniel E Neafsey, Marcelo U Ferreira
Author Information
Thaís C de Oliveira: Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil.
Priscila T Rodrigues: Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil.
Angela M Early: Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.
Ana Maria R C Duarte: Laboratory of Biochemistry and Molecular Biology, Superintendency for the Control of Endemics (SUCEN), State Secretary of Health, São Paulo, Brazil.
Julyana C Buery: Department of Social Medicine, Center for Health Sciences, Federal University of Espírito Santo, Vitória, Brazil.
Marina G Bueno: Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, Brazil.
José L Catão-Dias: Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, Brazil.
Crispim Cerutti: Department of Social Medicine, Center for Health Sciences, Federal University of Espírito Santo, Vitória, Brazil.
Luísa D P Rona: Department of Cell Biology, Embryology, and Genetics, Federal University of Santa Catarina, Florianópolis, Brazil.
Daniel E Neafsey: Infectious Disease and Microbiome Program, Broad Institute of MIT and Harvard, Cambridge, Massachusetts, USA.
Marcelo U Ferreira: Department of Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil. ORCID
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.