Advertisement

Origin of the New World Plasmodium vivax: Facts and New Approaches

  • R. Wiscovitch-RussoEmail author
  • Y. Narganes-Stordes
  • R. J. Cano
  • G. A. Toranzos
Original Article
  • 3 Downloads

Abstract

Malaria is one of the most important human diseases throughout tropical and sub-tropical regions of the world. Global distribution and ample host range have contributed to the genetic diversity of the etiological agent, Plasmodium. Phylogeographical analyses demonstrated that Plasmodium falciparum and Plasmodium vivax follow an Out of Africa (OOA) expansion, having a higher genetic diversity in African populations and a low genetic diversity in South American populations. Modeling the evolutionary rate of conserved genes for both P. falciparum and P. vivax determined the approximate arrival of human malaria in South America. Bayesian computational methods suggest that P. falciparum originated in Africa and arrived in South America through multiple independent introductions by the transatlantic African slave trade; however, in South America, P. vivax could have been introduced through an alternate migratory route. Alignments of P. vivax mitogenomes have revealed low genetic variation between the South American and Southeast Asian populations suggesting introduction through either pre-Columbian human migration or post-colonization events. To confirm the findings of these phylogeographical analyses, molecular methods were used to diagnose malaria infection in archeological remains of pre-Columbian ethnic groups. Immunohistochemistry tests were used and identified P. vivax but not P. falciparum in histologically prepared tissues from pre-Columbian Peruvian mummies, whereas shotgun metagenomics sequencing of DNA isolated from pre-Columbian Caribbean coprolites revealed Plasmodium-homologous reads; current evidence suggests that only P. vivax might have been present in pre-Columbian South America.

Keywords

P. falciparum P. vivax Malaria Pre-Columbian Phylogeography Paleoparasitology 

Notes

Funding information

This study was partially funded by the NIH RISE Program (NIH Grant No. 5R25GM061151–17).

Supplementary material

10123_2018_53_MOESM1_ESM.docx (11 kb)
ESM 1 (DOCX 11 kb)
10123_2018_53_MOESM2_ESM.docx (17 kb)
ESM 2 (DOCX 16 kb)
10123_2018_53_MOESM3_ESM.xlsx (155 kb)
ESM 3 (XLSX 154 kb)

References

  1. Anderson TJC, Haubold B, Williams JT, Estrada-Franco JG, Richardson L, Mollinedo R, Bockarie M, Mokili J, Mharakurwa S, French N, Whitworth J, Velez ID, Brockman AH, Nosten F, Ferreira MU, Day KP (2000) Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol 17:1467–1482CrossRefGoogle Scholar
  2. Arrow KJ, Panosian C, Gelband H (2004) Saving lives, buying time: economics of malaria drugs in an age of resistance. National Academies Press, Washington, D.CGoogle Scholar
  3. Ayala FJ, Escalante AA, Rich SM (1999) Evolution of Plasmodium and the recent origin of the world populations of Plasmodium falciparum. Parasitology 41:55–68Google Scholar
  4. Camargos Costa DC, Perreira de Assis GM, de Souza Silva FA, Araújo FC, de Souza Junior JC, Braga Hirano ZM, Kano FS, Nóbrega de Sousa T, Carvalho LH, de Brito CF (2015) Plasmodium simium, a Plasmodium vivax-related malaria parasite: genetic variability of Duffy binding protein II and the Duffy antigen/receptor for chemokines. PLoS One 10:1–16CrossRefGoogle Scholar
  5. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, Caler E, Crabtree J, Angiuoli SV, Merino EF, Amedeo P, Cheng Q, Coulson RMR, Fernandez-becerra C, Gilson PR, Gueye AH, Guo X, Kang S, Kooij TWA, Korsinczky M, Meyer EV, Nene V, Paulsen I, White O, Ralph SA, Ren Q, Sargeant TJ, Salzberg SL, Stoeckert CJ, Sullivan SA, Yamamoto MM, Hoffman SL, Wortman JR, Gardner MJ, Galinski MR, Barnwell JW, Fraser-liggett CM (2008) Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455:757–763CrossRefGoogle Scholar
  6. Carter R (2003) Speculations on the origins of Plasmodium vivax malaria. Trends Parasitol 19(5):214–219CrossRefGoogle Scholar
  7. Carter R, Mendis K (2002) Evolutionary and historical aspects of the burden of malaria. Clin Microbiol Rev 15:564–594CrossRefGoogle Scholar
  8. Clarkson C, Jacobs Z, Marwick B, Fullagar R, Wallis L, Smith M, Roberts RG, Hayes E, Lowe K, Carah X, Florin SA, McNeil J, Cox D, Arnold LJ, Hua Q, Huntley J, Brand HEA, Manne T, Fairbairn A, Shulmeister J, Lyle L, Salinas M, PageM CK, Park G, Norman K, Murphy T, Pardoe C (2017) Human occupation of northern Australia by 65,000 years ago. Nature 547(7663):306–310CrossRefGoogle Scholar
  9. Cleeland LM, Reichard MV, Tito RY, Reinhard KJ, Lewis CM (2013) Clarifying prehistoric parasitism form a complementary morphological and molecular approach. J Archaeol Sci 40(7):3060–3066CrossRefGoogle Scholar
  10. Crompton PD, Pierce SK, Miller LH (2010) Advances and challenges in malaria vaccine development. J Clin Invest 120:4166–4178CrossRefGoogle Scholar
  11. Der Sarkissian C, Allentoft ME, Avila-Arcos MC, Barnett R, Campos PF, Cappellini E, Ermini L, Fernandez R, da Fonseca R, Ginolhac A, Hansen AJ, Jonsson H, Korneliussen T, Margaryan A, Martin MD, Moreno-Mayar JV, Raghavan M, Rasmussen M, Sandoval Velasco M, Schroeder H, Schubert M, Seguin-Orlando A, Wales N, Gilbert MTP, Willerslev E, Orlando L (2015) Ancient genomics. Philos Trans R Soc Lond Ser B Biol Sci 370:20130387CrossRefGoogle Scholar
  12. Escalante AA, Ayala FJ (1995) Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes. Proc Natl Acad Sci U S A 92:5793–5797CrossRefGoogle Scholar
  13. Escalante AA, Barrio E, Ayala FJ (1995) Evolutionary origin of human and simian malarias: evidence from the circumsporozoite protein gene. Mol Biol Evol 12(4):616–626Google Scholar
  14. Escalante AA, Freeland DE, Collins WE, Lal AA (1998) The evolution of simian malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Proc Natl Acad Sci USA 95:8124–8129CrossRefGoogle Scholar
  15. Gerszten E, Allison MJ, Maguire B (2012) Paleopathology in south American mummies: a review and new findings. Pathobiology 79:247–256CrossRefGoogle Scholar
  16. Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci U S A 92:6723–6727CrossRefGoogle Scholar
  17. Good MF (2005) Vaccine-induced immunity to malaria parasites and the need for novel strategies. Immunoparasitol Ser 21(1):29–34Google Scholar
  18. Hart DL (2004) The origin of malaria: mixed messages from genetic diversity. Nat Rev Microbiol 2(1):15–22CrossRefGoogle Scholar
  19. Horuk R, Chitnis CE, Darbonne WC, Colby TC, Rybicki A, Hadley TJ, Miller LH (1993) A receptor for the malarial parasite Plasmodium vivax: the erythrocyte chemokine receptor. Science 261(5125):1182–1184CrossRefGoogle Scholar
  20. Howes RE, Patil AP, Piel FB, Nyangiri OA, Kabaria CW, Gething PW, Zimmerman PA, Barnadas C, Beall CM, Gebremedhin A, Ménard D, Williams TN, Weatherall DJ, Hay SI (2011) The global distribution of the Duffy blood group. Nat Commun 2:266CrossRefGoogle Scholar
  21. Jirků M, Pomajbíková K, Petrželková KJ, Hůzová Z, Modrý D, Lukeš J (2012) Detection of Plasmodium spp. in human feces. Emerg Infect Dis 18(4):634–636Google Scholar
  22. Joy DA, Feng X, Mu J, Furuya T, Chotivanich K, Krettli AU, Ho M, Wang A, White NJ, Suh E, Beerli P, Li X (2003) Early origin and recent expansion of Plasmodium falciparum. Science 300:318–321CrossRefGoogle Scholar
  23. Leclerc MC, Durand P, Gauthler C, Patot S, Billotte N, Menegon M, Severini C, Ayala FJ, Renaud F (2004a) Meager genetic variability of the human malaria agent Plasmodium vivax. Proc Natl Acad Sci U S A 101(40):14455–14460CrossRefGoogle Scholar
  24. Leclerc MC, Hugot JP, Durand P, Renaud F (2004b) Evolutionary relationships between 15 Plasmodium species from new and old world simians (including humans): an 18S rDNA cladistic analysis. Parasitology 129:677–684CrossRefGoogle Scholar
  25. Li J, Collins WE, Wirtz RA, Rathore D, Lal A, McCutchan F (2001) Geographic subdivision of the range of the malaria parasite Plasmodium vivax. Emerg Infect Dis 7(1):35–42CrossRefGoogle Scholar
  26. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Ndjango JN, Sanz CM, Morgan DB, Locatelli S, Gonder MK, Kranzusch PJ, Walsh PD, Delaporte E, Mpoudi-ngole E, Georgiev AV, Muller MN, Shaw GM, Peeters M, Sharp PM, Rayner JC, Hahn BH (2010) Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467(7314):420–425CrossRefGoogle Scholar
  27. 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 B, Ndjango JN, 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, Fa A, Bertolani P, Gillis A, Lebreton M, Tafon B, Kiyang J, Djoko CF, Schneider BS, Wolfe ND, Mpoudi-ngole E, Delaporte E, Carter R, Richard L, Shaw GM, Rayner JC, Peeters M, Hahn BH, Sharp PM (2014) African origin of the malaria parasite Plasmodium vivax. Nat Commun 5:3346.  https://doi.org/10.1038/ncomms4346 CrossRefGoogle Scholar
  28. Mita T, Tanabe K, Kita K (2009) Spread and evolution of Plasmodium falciparum drug resistance. Parasitol Int 58:201–209CrossRefGoogle Scholar
  29. Neafsey DE, Schaffner SF, Volkman SK, Park D, Montgomery P, Milner DA, Lukens A, Rosen D, Daniels R, Houde N, Cortese JF, Tyndall E, Gates C, Stange-Thomann N, Sarr O, Ndiaye D, Ndir O, Mboup S, Ferreira MU, Moraes S do L, Dash AP, Chitnis CE, Wiegand RC, Hartl DL, Birren BW, Lander ES, Sabeti PC, Wirth DF (2008) Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol 9(12):R171–R1712CrossRefGoogle Scholar
  30. Otto TD, Rayner JC, Bohme U, Pain A, Spottiswoode N, Sanders M, Quail M, Ollomo B, Renaud F, Thomas AW, Prugnolle F, Conway DJ, Newbold C, Berriman M (2014) Genome sequencing of chimpanzee malaria parasites reveals possible pathways of adaptation to human hosts. Nat Commun 5:4754CrossRefGoogle Scholar
  31. Pääbo S (1989) Ancient DNA: extraction, characterization, molecular cloning, and enzymatic amplification. Proc Natl Acad Sci U S A 86:1939–1943CrossRefGoogle Scholar
  32. Prugnolle F, Rougeron V, Becquart P, Berry A, Makanga B, Rahola N, Arnathau C, Ngoubangoye B, Menard S, Willaume E, Ayala FJ, Fontenille F, Ollomo B, Durand P, Paupy C, Renaud F (2013) Diversity, host switching and evolution of Plasmodium vivax infecting African great apes. Proc Natl Acad Sci U S A 110:8123–8128CrossRefGoogle Scholar
  33. Rich SM, Leendertz FH, Xu G, LeBreton M, Djoko CF, Aminake MN, Takang EE, Diffo JL, Pike BL, Rosenthal BM, Formenty P, Boesch C, Ayala FJ, Wolfe ND (2009) The origin of malignant malaria. Proc Natl Acad Sci U S A 106:14902–14907CrossRefGoogle Scholar
  34. Rivera-Perez JI, Cano RJ, Narganes-Storde Y, Chanlatte-Baik L, Toranzos GA (2015) Retroviral DNA sequences as a means for determining ancient diets. PLoS One 10:1–10CrossRefGoogle Scholar
  35. Rodrigues PT, Valdivia HO, de Oliveira T, Alves JMP, Duarte AMRC, Duarte AMRC, Cerutti-Junior C, Buery JC, Brito CFA, de Souza JC Jr, Hirano ZMB, Bueno MG, Catão-dias JL, Malafronte RS, Ladeia-Andrade S, Mita T, Santamaria AM, Calzada JE, Tantular IS, Kawamoto F, Raijmakers LRJ, Mueller I, Pacheco MA, Escalante AA, Felger I, Ferreira MU (2018) Human migration and the spread of malaria parasites to the New World. Nat Sci Rep 8:1993.  https://doi.org/10.1038/s41598-018-19554-0 CrossRefGoogle Scholar
  36. Sharp PM, Liu W, Learn GH, Rayner JC, Peeters M, Hahn BH (2011) Source of the human malaria parasite Plasmodium falciparum. Proc Natl Acad Sci 108(38):E744–E745CrossRefGoogle Scholar
  37. Søe MJ, Nejsum P, Fredensborg BL, Kapel CM (2015) DNA typing of ancient parasite eggs from environmental samples identifies human and animal worm infections in Viking-age settlement. J Parasitol 101(1):57–63CrossRefGoogle Scholar
  38. Tanabe K, Mita T, Jombart T, Eriksson A, Horibe S, Palacpac N, Ranford-Cartwright L, Sawai H, Sakihama N, Ohmae H, Nakamura M, Ferreira MU, Escalante AA, Prugnolle F, Björkman A, Färnert A, Kaneko A, Horii T, Manica A, Kishino H, Balloux F (2010) Plasmodium falciparum accompanied the human expansion out of Africa. Curr Biol 20:1283–1289CrossRefGoogle Scholar
  39. Taylor JE, Pacheco MA, Bacon DJ, Beg MA, Machado RL, Fairhurst RM, Herrera S, Kim JY, Menard D, Póvoa MM, Villegas L, Mulyanto SG, Cui L, Zeyrek FY, Escalante AA (2013) The evolutionary history of Plasmodium vivax as inferred from mitochondrial genomes: parasite genetic diversity in the Americas. Mol Biol Evol 30(9):2050–2064CrossRefGoogle Scholar
  40. Tito RY, Macmil S, Wiley G, Najar F, Cleeland L, Qu C, Wang P, Romagne F, Leonard S, Jimenez Ruiz A, Reinhard K, Roe BA, Lewis CM (2008) Phylotyping and functional analysis of two ancient human microbiomes. PLoS One 3(11):e3703Google Scholar
  41. Tournamille C, Colin Y, Carton JP, Le Van Kim C (1995) Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy-negative individuals. Nat Gen 10:224–228CrossRefGoogle Scholar
  42. Vinayak S, Alam MT, Mixson-Hayden T, McCollum AM, Sem R, Shah NK, Lim P, Muth S, Rogers WO, Fandeur T, Barnwell JW, Escalante AA, Wongsrichanalai C, Ariey F, Meshnick SR, Udhayakumar V (2010) Origin and evolution of sulfadoxine resistant Plasmodium falciparum. PLoS Pathog 6(3):e1000830CrossRefGoogle Scholar
  43. Yalcindag E, Elguero E, Arnathau C, Durand P, Akiana J, Anderson TTJ, Aubouy A, Balloux F, Besnard P, Bogreau H, Carnevale P, D’Alessandro U, Fontenille D, Gamboa D, Jombart T, Le Mire J, Leroy E, Maestre A, Mayxay M, Ménard D, Musset L, Newton PPN, Nkoghé D, Noya O, Ollomo B, Rogier C, Veron V, Wide A, Zakeri S, Carme B, Legrand E, Chevillon C, Ayala FJF, Renaud F, Prugnolle F (2012) Multiple independent introductions of Plasmodium falciparum in South America. Proc Natl Acad Sci 109(2):511–516CrossRefGoogle Scholar
  44. Yamasaki T, Duarte AM, Curado I, Summa ME, Neves DV, Wunderlich G, Malafronte RS (2011) Detection of etiological agents of malaria in howler monkeys from Atlantic forests, rescued in regions of São Paulo City, Brazil. J Med Primatol 40(6):392–400CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Environmental Microbiology LaboratoryUniversity of Puerto RicoSan JuanUSA
  2. 2.Department of BiologyUniversity of Puerto RicoSan JuanUSA
  3. 3.Center for Archaeological ResearchUniversity of Puerto RicoSan JuanUSA
  4. 4.The BioCollectiveDenverUSA

Personalised recommendations