African origin of the malaria parasite Plasmodium vivax

Weimin Liu; Yingying Li; Katharina S. Shaw; Gerald H. Learn; Lindsey J. Plenderleith; Jordan A. Malenke; Sesh A. Sundararaman; Miguel A. Ramirez; Patricia A. Crystal; Andrew G. Smith; Frederic Bibollet-Ruche; Ahidjo Ayouba; Sabrina Locatelli; Amandine Esteban; Fatima Mouacha; Emilande Guichet; Christelle Butel; Steve Ahuka-Mundeke; Bila Isia Inogwabini; Jean Bosco N. Ndjango; Sheri Speede; Crickette M. Sanz; David B. Morgan; Mary K. Gonder; Philip J. Kranzusch; Peter D. Walsh; Alexander V. Georgiev; Martin N. Muller; Alex K. Piel; Fiona A. Stewart; Michael L. Wilson; Anne E. Pusey; Liwang Cui; Zenglei Wang; Anna Färnert; Colin J. Sutherland; Debbie Nolder; John A. Hart; Terese B. Hart; Paco Bertolani; Amethyst Gillis; Matthew LeBreton; Babila Tafon; John Kiyang; Cyrille F. Djoko; Bradley S. Schneider; Nathan D. Wolfe; Eitel Mpoudi-Ngole; Eric Delaporte; Richard Carter; Richard L. Culleton; George M. Shaw; Julian C. Rayner; Martine Peeters; Beatrice H. Hahn; Paul M. Sharp

doi:10.1038/ncomms4346

African origin of the malaria parasite Plasmodium vivax

Weimin Liu, Yingying Li, Katharina S. Shaw, Gerald H. Learn, Lindsey J. Plenderleith, Jordan A. Malenke, Sesh A. Sundararaman, Miguel A. Ramirez, Patricia A. Crystal, Andrew G. Smith, Frederic Bibollet-Ruche, Ahidjo Ayouba, Sabrina Locatelli, Amandine Esteban, Fatima Mouacha, Emilande Guichet, Christelle Butel, Steve Ahuka-Mundeke, Bila Isia Inogwabini, Jean Bosco N. NdjangoSheri Speede, Crickette M. Sanz, David B. Morgan, Mary K. Gonder, Philip J. Kranzusch, Peter D. Walsh, Alexander V. Georgiev, Martin N. Muller, Alex K. Piel, Fiona A. Stewart, Michael L. Wilson, Anne E. Pusey, Liwang Cui, Zenglei Wang, Anna Färnert, Colin J. Sutherland, Debbie Nolder, John A. Hart, Terese B. Hart, Paco Bertolani, Amethyst Gillis, Matthew LeBreton, Babila Tafon, John Kiyang, Cyrille F. Djoko, Bradley S. Schneider, Nathan D. Wolfe, Eitel Mpoudi-Ngole, Eric Delaporte, Richard Carter, Richard L. Culleton, George M. Shaw, Julian C. Rayner, Martine Peeters, Beatrice H. Hahn, Paul M. Sharp

Entomology

Research output: Contribution to journal › Article › peer-review

119 Scopus citations

Abstract

Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.

Original language	English (US)
Article number	3346
Journal	Nature communications
Volume	5
DOIs	https://doi.org/10.1038/ncomms4346
State	Published - Feb 21 2014

All Science Journal Classification (ASJC) codes

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

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Liu, W., Li, Y., Shaw, K. S., Learn, G. H., Plenderleith, L. J., Malenke, J. A., Sundararaman, S. A., Ramirez, M. A., Crystal, P. A., Smith, A. G., Bibollet-Ruche, F., Ayouba, A., Locatelli, S., Esteban, A., Mouacha, F., Guichet, E., Butel, C., Ahuka-Mundeke, S., Inogwabini, B. I., ... Sharp, P. M. (2014). African origin of the malaria parasite Plasmodium vivax. Nature communications, 5, [3346]. https://doi.org/10.1038/ncomms4346

Liu, Weimin ; Li, Yingying ; Shaw, Katharina S. ; Learn, Gerald H. ; Plenderleith, Lindsey J. ; Malenke, Jordan A. ; Sundararaman, Sesh A. ; Ramirez, Miguel A. ; Crystal, Patricia A. ; Smith, Andrew G. ; Bibollet-Ruche, Frederic ; Ayouba, Ahidjo ; Locatelli, Sabrina ; Esteban, Amandine ; Mouacha, Fatima ; Guichet, Emilande ; Butel, Christelle ; Ahuka-Mundeke, Steve ; Inogwabini, Bila Isia ; Ndjango, Jean Bosco N. ; Speede, Sheri ; Sanz, Crickette M. ; Morgan, David B. ; Gonder, Mary K. ; Kranzusch, Philip J. ; Walsh, Peter D. ; Georgiev, Alexander V. ; Muller, Martin N. ; Piel, Alex K. ; Stewart, Fiona A. ; Wilson, Michael L. ; Pusey, Anne E. ; Cui, Liwang ; Wang, Zenglei ; Färnert, Anna ; Sutherland, Colin J. ; Nolder, Debbie ; Hart, John A. ; Hart, Terese B. ; Bertolani, Paco ; Gillis, Amethyst ; LeBreton, Matthew ; Tafon, Babila ; Kiyang, John ; Djoko, Cyrille F. ; Schneider, Bradley S. ; Wolfe, Nathan D. ; Mpoudi-Ngole, Eitel ; Delaporte, Eric ; Carter, Richard ; Culleton, Richard L. ; Shaw, George M. ; Rayner, Julian C. ; Peeters, Martine ; Hahn, Beatrice H. ; Sharp, Paul M. / African origin of the malaria parasite Plasmodium vivax. In: Nature communications. 2014 ; Vol. 5.

@article{07374b3b621c46ce948f1525bfe50fdb,

title = "African origin of the malaria parasite Plasmodium vivax",

abstract = "Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.",

author = "Weimin Liu and Yingying Li and Shaw, {Katharina S.} and Learn, {Gerald H.} and Plenderleith, {Lindsey J.} and Malenke, {Jordan A.} and Sundararaman, {Sesh A.} and Ramirez, {Miguel A.} and Crystal, {Patricia A.} and Smith, {Andrew G.} and Frederic Bibollet-Ruche and Ahidjo Ayouba and Sabrina Locatelli and Amandine Esteban and Fatima Mouacha and Emilande Guichet and Christelle Butel and Steve Ahuka-Mundeke and Inogwabini, {Bila Isia} and Ndjango, {Jean Bosco N.} and Sheri Speede and Sanz, {Crickette M.} and Morgan, {David B.} and Gonder, {Mary K.} and Kranzusch, {Philip J.} and Walsh, {Peter D.} and Georgiev, {Alexander V.} and Muller, {Martin N.} and Piel, {Alex K.} and Stewart, {Fiona A.} and Wilson, {Michael L.} and Pusey, {Anne E.} and Liwang Cui and Zenglei Wang and Anna F{\"a}rnert and Sutherland, {Colin J.} and Debbie Nolder and Hart, {John A.} and Hart, {Terese B.} and Paco Bertolani and Amethyst Gillis and Matthew LeBreton and Babila Tafon and John Kiyang and Djoko, {Cyrille F.} and Schneider, {Bradley S.} and Wolfe, {Nathan D.} and Eitel Mpoudi-Ngole and Eric Delaporte and Richard Carter and Culleton, {Richard L.} and Shaw, {George M.} and Rayner, {Julian C.} and Martine Peeters and Hahn, {Beatrice H.} and Sharp, {Paul M.}",

note = "Funding Information: We thank the staff of project PRESICA, the World Wildlife Fund for Nature (WWF/ DRC), the Institut National de Recherches Biom{\'e}dicales (INRB, Kinshasa, DRC), Global Viral Cameroon, the Bonobo Conservation Initiative and Vie Sauvage, as well as Didier Mazongo, Octavie Lunguya, Muriel Aloni and Valentin Mbenz for fieldwork in Cameroon and the DRC; field assistants in Gombe National Park and Ugalla for sample collection in Tanzania, the staff of the Sanaga Yong, Limbe and Ape Action Africa/Mfou National Park Wildlife Rescue Centres for collecting blood samples from captive apes; the Cameroonian Ministries of Health, Forestry and Wildlife, and Scientific Research and Innovation for permission to collect samples in Cameroon; the Water and Forest Ministry for permission to collect samples in the Central African Republic; the Ministry of Forest Economy and Sustainable Development for permission to collect samples in the Republic of Congo; the Ministry of Scientific Research and Technology, the Department of Ecology and Management of Plant and Animal Resources of the University of Kisangani, the Ministries of Health and Environment and the National Ethics Committee for permission to collect samples in the DRC; the Tanzania Commission for Science and Technology and the Tanzania Wildlife Research Institute for permission to conduct research in Gombe National Park and Ugalla. This work was supported by grants from the National Institutes of Health (R01 AI091595, R37 AI050529, R01 AI58715, T32 AI007532, P30 AI045008), the Agence Nationale de Recherche sur le Sida (ANRS 12125/ 12182/12255), the Agence Nationale de Recherche (Programme Blanc, Sciences de la Vie, de la Sant{\'e} et des Ecosyst{\'e}mes and ANR 11 BSV3 021 01, Projet PRIMAL), Harvard University, the Arthur L. Greene Fund, the Jane Goodall Institute, the Wellcome Trust (098051), the Leakey Foundation, Google.org and the Skoll Foundation. This study was also made possible by the generous support of the American people through the United States Agency for International Development (USAID) Emerging Pandemic Threats PREDICT. The contents are the responsibility of the authors and do not necessarily reflect the views of USAID or the United States Government.",

year = "2014",

month = feb,

day = "21",

doi = "10.1038/ncomms4346",

language = "English (US)",

volume = "5",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Nature Publishing Group",

}

Liu, W, Li, Y, Shaw, KS, Learn, GH, Plenderleith, LJ, Malenke, JA, Sundararaman, SA, Ramirez, MA, Crystal, PA, Smith, AG, Bibollet-Ruche, F, Ayouba, A, Locatelli, S, Esteban, A, Mouacha, F, Guichet, E, Butel, C, Ahuka-Mundeke, S, Inogwabini, BI, Ndjango, JBN, Speede, S, Sanz, CM, Morgan, DB, Gonder, MK, Kranzusch, PJ, Walsh, PD, Georgiev, AV, Muller, MN, Piel, AK, Stewart, FA, Wilson, ML, Pusey, AE, Cui, L, Wang, Z, Färnert, A, Sutherland, CJ, Nolder, D, Hart, JA, Hart, TB, Bertolani, P, Gillis, A, LeBreton, M, Tafon, B, Kiyang, J, Djoko, CF, Schneider, BS, Wolfe, ND, Mpoudi-Ngole, E, Delaporte, E, Carter, R, Culleton, RL, Shaw, GM, Rayner, JC, Peeters, M, Hahn, BH & Sharp, PM 2014, 'African origin of the malaria parasite Plasmodium vivax', Nature communications, vol. 5, 3346. https://doi.org/10.1038/ncomms4346

African origin of the malaria parasite Plasmodium vivax. / Liu, Weimin; Li, Yingying; Shaw, Katharina S.; Learn, Gerald H.; Plenderleith, Lindsey J.; Malenke, Jordan A.; Sundararaman, Sesh A.; Ramirez, Miguel A.; Crystal, Patricia A.; Smith, Andrew G.; Bibollet-Ruche, Frederic; Ayouba, Ahidjo; Locatelli, Sabrina; Esteban, Amandine; Mouacha, Fatima; Guichet, Emilande; Butel, Christelle; Ahuka-Mundeke, Steve; Inogwabini, Bila Isia; Ndjango, Jean Bosco N.; Speede, Sheri; Sanz, Crickette M.; Morgan, David B.; Gonder, Mary K.; Kranzusch, Philip J.; Walsh, Peter D.; Georgiev, Alexander V.; Muller, Martin N.; Piel, Alex K.; Stewart, Fiona A.; Wilson, Michael L.; Pusey, Anne E.; Cui, Liwang; Wang, Zenglei; Färnert, Anna; Sutherland, Colin J.; Nolder, Debbie; Hart, John A.; Hart, Terese B.; Bertolani, Paco; Gillis, Amethyst; LeBreton, Matthew; Tafon, Babila; Kiyang, John; Djoko, Cyrille F.; Schneider, Bradley S.; Wolfe, Nathan D.; Mpoudi-Ngole, Eitel; Delaporte, Eric; Carter, Richard; Culleton, Richard L.; Shaw, George M.; Rayner, Julian C.; Peeters, Martine; Hahn, Beatrice H.; Sharp, Paul M.

In: Nature communications, Vol. 5, 3346, 21.02.2014.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - African origin of the malaria parasite Plasmodium vivax

AU - Liu, Weimin

AU - Li, Yingying

AU - Shaw, Katharina S.

AU - Learn, Gerald H.

AU - Plenderleith, Lindsey J.

AU - Malenke, Jordan A.

AU - Sundararaman, Sesh A.

AU - Ramirez, Miguel A.

AU - Crystal, Patricia A.

AU - Smith, Andrew G.

AU - Bibollet-Ruche, Frederic

AU - Ayouba, Ahidjo

AU - Locatelli, Sabrina

AU - Esteban, Amandine

AU - Mouacha, Fatima

AU - Guichet, Emilande

AU - Butel, Christelle

AU - Ahuka-Mundeke, Steve

AU - Inogwabini, Bila Isia

AU - Ndjango, Jean Bosco N.

AU - Speede, Sheri

AU - Sanz, Crickette M.

AU - Morgan, David B.

AU - Gonder, Mary K.

AU - Kranzusch, Philip J.

AU - Walsh, Peter D.

AU - Georgiev, Alexander V.

AU - Muller, Martin N.

AU - Piel, Alex K.

AU - Stewart, Fiona A.

AU - Wilson, Michael L.

AU - Pusey, Anne E.

AU - Cui, Liwang

AU - Wang, Zenglei

AU - Färnert, Anna

AU - Sutherland, Colin J.

AU - Nolder, Debbie

AU - Hart, John A.

AU - Hart, Terese B.

AU - Bertolani, Paco

AU - Gillis, Amethyst

AU - LeBreton, Matthew

AU - Tafon, Babila

AU - Kiyang, John

AU - Djoko, Cyrille F.

AU - Schneider, Bradley S.

AU - Wolfe, Nathan D.

AU - Mpoudi-Ngole, Eitel

AU - Delaporte, Eric

AU - Carter, Richard

AU - Culleton, Richard L.

AU - Shaw, George M.

AU - Rayner, Julian C.

AU - Peeters, Martine

AU - Hahn, Beatrice H.

AU - Sharp, Paul M.

N1 - Funding Information: We thank the staff of project PRESICA, the World Wildlife Fund for Nature (WWF/ DRC), the Institut National de Recherches Biomédicales (INRB, Kinshasa, DRC), Global Viral Cameroon, the Bonobo Conservation Initiative and Vie Sauvage, as well as Didier Mazongo, Octavie Lunguya, Muriel Aloni and Valentin Mbenz for fieldwork in Cameroon and the DRC; field assistants in Gombe National Park and Ugalla for sample collection in Tanzania, the staff of the Sanaga Yong, Limbe and Ape Action Africa/Mfou National Park Wildlife Rescue Centres for collecting blood samples from captive apes; the Cameroonian Ministries of Health, Forestry and Wildlife, and Scientific Research and Innovation for permission to collect samples in Cameroon; the Water and Forest Ministry for permission to collect samples in the Central African Republic; the Ministry of Forest Economy and Sustainable Development for permission to collect samples in the Republic of Congo; the Ministry of Scientific Research and Technology, the Department of Ecology and Management of Plant and Animal Resources of the University of Kisangani, the Ministries of Health and Environment and the National Ethics Committee for permission to collect samples in the DRC; the Tanzania Commission for Science and Technology and the Tanzania Wildlife Research Institute for permission to conduct research in Gombe National Park and Ugalla. This work was supported by grants from the National Institutes of Health (R01 AI091595, R37 AI050529, R01 AI58715, T32 AI007532, P30 AI045008), the Agence Nationale de Recherche sur le Sida (ANRS 12125/ 12182/12255), the Agence Nationale de Recherche (Programme Blanc, Sciences de la Vie, de la Santé et des Ecosystémes and ANR 11 BSV3 021 01, Projet PRIMAL), Harvard University, the Arthur L. Greene Fund, the Jane Goodall Institute, the Wellcome Trust (098051), the Leakey Foundation, Google.org and the Skoll Foundation. This study was also made possible by the generous support of the American people through the United States Agency for International Development (USAID) Emerging Pandemic Threats PREDICT. The contents are the responsibility of the authors and do not necessarily reflect the views of USAID or the United States Government.

PY - 2014/2/21

Y1 - 2014/2/21

N2 - Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.

AB - Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.

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