September 22, 2019  |  

Evolutionary history of human Plasmodium vivax revealed by genome-wide analyses of related ape parasites.

Authors: Loy, Dorothy E and Plenderleith, Lindsey J and Sundararaman, Sesh A and Liu, Weimin and Gruszczyk, Jakub and Chen, Yi-Jun and Trimboli, Stephanie and Learn, Gerald H and MacLean, Oscar A and Morgan, Alex L K and Li, Yingying and Avitto, Alexa N and Giles, Jasmin and Calvignac-Spencer, Sébastien and Sachse, Andreas and Leendertz, Fabian H and Speede, Sheri and Ayouba, Ahidjo and Peeters, Martine and Rayner, Julian C and Tham, Wai-Hong and Sharp, Paul M and Hahn, Beatrice H

Wild-living African apes are endemically infected with parasites that are closely related to human Plasmodium vivax, a leading cause of malaria outside Africa. This finding suggests that the origin of P. vivax was in Africa, even though the parasite is now rare in humans there. To elucidate the emergence of human P. vivax and its relationship to the ape parasites, we analyzed genome sequence data of P. vivax strains infecting six chimpanzees and one gorilla from Cameroon, Gabon, and Côte d'Ivoire. We found that ape and human parasites share nearly identical core genomes, differing by only 2% of coding sequences. However, compared with the ape parasites, human strains of P. vivax exhibit about 10-fold less diversity and have a relative excess of nonsynonymous nucleotide polymorphisms, with site-frequency spectra suggesting they are subject to greatly relaxed purifying selection. These data suggest that human P. vivax has undergone an extreme bottleneck, followed by rapid population expansion. Investigating potential host-specificity determinants, we found that ape P. vivax parasites encode intact orthologs of three reticulocyte-binding protein genes (rbp2d, rbp2e, and rbp3), which are pseudogenes in all human P. vivax strains. However, binding studies of recombinant RBP2e and RBP3 proteins to human, chimpanzee, and gorilla erythrocytes revealed no evidence of host-specific barriers to red blood cell invasion. These data suggest that, from an ancient stock of P. vivax parasites capable of infecting both humans and apes, a severely bottlenecked lineage emerged out of Africa and underwent rapid population growth as it spread globally. Copyright © 2018 the Author(s). Published by PNAS.

Journal: Proceedings of the National Academy of Sciences of the United States of America
DOI: 10.1073/pnas.1810053115
Year: 2018

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