1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Malaria Molecular Epidemiology: An Evolutionary Genetics Perspective *

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • Authors: Ananias A. Escalante1, M. Andreína Pacheco2
  • Editors: Lee W. Riley3, Ronald E. Blanton4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Department of Biology/Institute for Genomics and Evolutionary Medicine, Temple University, Philadelphia, PA 19122; 2: Department of Biology/Institute for Genomics and Evolutionary Medicine, Temple University, Philadelphia, PA 19122; 3: Divisions of Infectious Diseases and Vaccinology, School of Public Health, University of California, Berkeley, Berkeley, CA; 4: Center for Global Health & Diseases, Case Western Reserve University, Cleveland, OH
  • Source: microbiolspec August 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.AME-0010-2019
  • Received 08 May 2019 Accepted 23 May 2019 Published 09 August 2019
  • Ananias A. Escalante, [email protected]
image of Malaria Molecular Epidemiology: An Evolutionary Genetics Perspective<span class="xref">
<a href="#fn1">*</a>
</span>
    Preview this microbiology spectrum article:
    Zoom in
    Zoomout

    Malaria Molecular Epidemiology: An Evolutionary Genetics Perspective * , Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/7/4/AME-0010-2019-1.gif /docserver/preview/fulltext/microbiolspec/7/4/AME-0010-2019-2.gif
  • Abstract:

    Malaria is a vector-borne disease that involves multiple parasite species in a variety of ecological settings. However, the parasite species causing the disease, the prevalence of subclinical infections, the emergence of drug resistance, the scale-up of interventions, and the ecological factors affecting malaria transmission, among others, are aspects that vary across areas where malaria is endemic. Such complexities have propelled the study of parasite genetic diversity patterns in the context of epidemiologic investigations. Importantly, molecular studies indicate that the time and spatial distribution of malaria cases reflect epidemiologic processes that cannot be fully understood without characterizing the evolutionary forces shaping parasite population genetic patterns. Although broad in scope, this review in the Curated Collection: Advances in Molecular Epidemiology highlights the need for understanding population genetic concepts when interpreting parasite molecular data. First, we discuss malaria complexity in terms of the parasite species involved. Second, we describe how molecular data are changing our understanding of malaria incidence and infectiousness. Third, we compare different approaches to generate parasite genetic information in the context of epidemiologically relevant questions related to malaria control. Finally, we describe a few genomic studies as evidence of how these approaches will provide new insights into the malaria disease dynamics.

    *This article is part of a curated collection.

  • Citation: Escalante A, Pacheco M. 2019. Malaria Molecular Epidemiology: An Evolutionary Genetics Perspective * . Microbiol Spectrum 7(4):AME-0010-2019. doi:10.1128/microbiolspec.AME-0010-2019.

References

1. World Health Organization. 2018. World Malaria Report 2018. World Health Organization, Geneva, Switzerland. https://www.who.int/malaria/publications/world-malaria-report-2018/en/.
2. Coatney RG, Collins WE, Warren M, Contacos PG. 1971. The Primate Malaria. US Government Printing Office, Washington, DC.
3. Escalante AA, Cornejo OE, Freeland DE, Poe AC, Durrego E, Collins WE, Lal AA. 2005. A monkey’s tale: the origin of Plasmodium vivax as a human malaria parasite. Proc Natl Acad Sci U S A 102:1980–1985. http://dx.doi.org/10.1073/pnas.0409652102. [PubMed]
4. Muehlenbein MP, Pacheco MA, Taylor JE, Prall SP, Ambu L, Nathan S, Alsisto S, Ramirez D, Escalante AA. 2015. Accelerated diversification of nonhuman primate malarias in Southeast Asia: adaptive radiation or geographic speciation? Mol Biol Evol 32:422–439. http://dx.doi.org/10.1093/molbev/msu310. [PubMed]
5. Otto TD, Rayner JC, Böhme 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 5:4754. http://dx.doi.org/10.1038/ncomms5754. [PubMed]
6. Gilabert A, Otto TD, Rutledge GG, Franzon B, Ollomo B, Arnathau C, Durand P, Moukodoum ND, Okouga AP, Ngoubangoye B, Makanga B, Boundenga L, Paupy C, Renaud F, Prugnolle F, Rougeron V. 2018. Plasmodium vivax-like genome sequences shed new insights into Plasmodium vivax biology and evolution. PLoS Biol 16:e2006035. http://dx.doi.org/10.1371/journal.pbio.2006035. [PubMed]
7. Loy DE, Plenderleith LJ, Sundararaman SA, Liu W, Gruszczyk J, Chen YJ, Trimboli S, Learn GH, MacLean OA, Morgan ALK, Li Y, Avitto AN, Giles J, Calvignac-Spencer S, Sachse A, Leendertz FH, Speede S, Ayouba A, Peeters M, Rayner JC, Tham WH, Sharp PM, Hahn BH. 2018. Evolutionary history of human Plasmodium vivax revealed by genome-wide analyses of related ape parasites. Proc Natl Acad Sci U S A 115:E8450–E8459. http://dx.doi.org/10.1073/pnas.1810053115. [PubMed]
8. Bousema T, Drakeley C. 2011. Epidemiology and infectivity of Plasmodium falciparum and Plasmodium vivax gametocytes in relation to malaria control and elimination. Clin Microbiol Rev 24:377–410. http://dx.doi.org/10.1128/CMR.00051-10. [PubMed]
9. Schneider KA, Escalante AA. 2013. Fitness components and natural selection: why are there different patterns on the emergence of drug resistance in Plasmodium falciparum and Plasmodium vivax? Malar J 12:15. http://dx.doi.org/10.1186/1475-2875-12-15. [PubMed]
10. Wahlgren M, Goel S, Akhouri RR. 2017. Variant surface antigens of Plasmodium falciparum and their roles in severe malaria. Nat Rev Microbiol 15:479–491. http://dx.doi.org/10.1038/nrmicro.2017.47. [PubMed]
11. Wassmer SC, Taylor TE, Rathod PK, Mishra SK, Mohanty S, Arevalo-Herrera M, Duraisingh MT, Smith JD. 2015. Investigating the pathogenesis of severe malaria: a multidisciplinary and cross-geographical approach. Am J Trop Med Hyg 93(Suppl) :42–56. http://dx.doi.org/10.4269/ajtmh.14-0841. [PubMed]
12. Mayor A, Bardají A, Macete E, Nhampossa T, Fonseca AM, González R, Maculuve S, Cisteró P, Rupérez M, Campo J, Vala A, Sigaúque B, Jiménez A, Machevo S, de la Fuente L, Nhama A, Luis L, Aponte JJ, Acácio S, Nhacolo A, Chitnis C, Dobaño C, Sevene E, Alonso PL, Menéndez C. 2015. Changing trends in P. falciparum burden, immunity, and disease in pregnancy. N Engl J Med 373:1607–1617. http://dx.doi.org/10.1056/NEJMoa1406459. [PubMed]
13. Arevalo-Herrera M, Quiñones ML, Guerra C, Céspedes N, Giron S, Ahumada M, Piñeros JG, Padilla N, Terrientes Z, Rosas A, Padilla JC, Escalante AA, Beier JC, Herrera S. 2012. Malaria in selected non-Amazonian countries of Latin America. Acta Trop 121:303–314. http://dx.doi.org/10.1016/j.actatropica.2011.06.008. [PubMed]
14. Hay SI, Snow RW. 2006. The malaria Atlas Project: developing global maps of malaria risk. PLoS Med 3:e473. http://dx.doi.org/10.1371/journal.pmed.0030473. [PubMed]
15. Chowell G, Munayco CV, Escalante AA, McKenzie FE. 2009. The spatial and temporal patterns of falciparum and vivax malaria in Perú: 1994–2006. Malar J 8:142. http://dx.doi.org/10.1186/1475-2875-8-142. [PubMed]
16. Singh B, Kim Sung L, Matusop A, Radhakrishnan A, Shamsul SS, Cox-Singh J, Thomas A, Conway DJ. 2004. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet 363:1017–1024. http://dx.doi.org/10.1016/S0140-6736(04)15836-4.
17. Yusof R, Ahmed MA, Jelip J, Ngian HU, Mustakim S, Hussin HM, Fong MY, Mahmud R, Sitam FA, Japning JR, Snounou G, Escalante AA, Lau YL. 2016. Phylogeographic evidence for 2 genetically distinct zoonotic Plasmodium knowlesi parasites, Malaysia. Emerg Infect Dis 22:1371–1380. http://dx.doi.org/10.3201/eid2208.151885. [PubMed]
18. William T, Jelip J, Menon J, Anderios F, Mohammad R, Awang Mohammad TA, Grigg MJ, Yeo TW, Anstey NM, Barber BE. 2014. Changing epidemiology of malaria in Sabah, Malaysia: increasing incidence of Plasmodium knowlesi. Malar J 13:390. http://dx.doi.org/10.1186/1475-2875-13-390. [PubMed]
19. Ta TH, Hisam S, Lanza M, Jiram AI, Ismail N, Rubio JM. 2014. First case of a naturally acquired human infection with Plasmodium cynomolgi. Malar J 13:68. http://dx.doi.org/10.1186/1475-2875-13-68. [PubMed]
20. Imwong M, Madmanee W, Suwannasin K, Kunasol C, Peto TJ, Tripura R, von Seidlein L, Nguon C, Davoeung C, Day NPJ, Dondorp AM, White NJ. 2019. Asymptomatic natural human infections with the simian malaria parasites Plasmodium cynomolgi and Plasmodium knowlesi. J Infect Dis 219:695–702. http://dx.doi.org/10.1093/infdis/jiy519. [PubMed]
21. Lalremruata A, Magris M, Vivas-Martínez S, Koehler M, Esen M, Kempaiah P, Jeyaraj S, Perkins DJ, Mordmüller B, Metzger WG. 2015. Natural infection of Plasmodium brasilianum in humans: man and monkey share quartan malaria parasites in the Venezuelan Amazon. EBioMedicine 2:1186–1192. http://dx.doi.org/10.1016/j.ebiom.2015.07.033. [PubMed]
22. Brasil P, Zalis MG, de Pina-Costa A, Siqueira AM, Júnior CB, Silva S, Areas ALL, Pelajo-Machado M, de Alvarenga DAM, da Silva Santelli ACF, Albuquerque HG, Cravo P, Santos de Abreu FV, Peterka CL, Zanini GM, Suárez Mutis MC, Pissinatti A, Lourenço-de-Oliveira R, de Brito CFA, de Fátima Ferreira-da-Cruz M, Culleton R, Daniel-Ribeiro CT. 2017. Outbreak of human malaria caused by Plasmodium simium in the Atlantic Forest in Rio de Janeiro: a molecular epidemiological investigation. Lancet Glob Health 5:e1038–e1046. http://dx.doi.org/10.1016/S2214-109X(17)30333-9.
23. Escalante AA, Barrio E, Ayala FJ. 1995. Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene. Mol Biol Evol 12:616–626.
24. Pacheco MA, Cranfield M, Cameron K, Escalante AA. 2013. Malarial parasite diversity in chimpanzees: the value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens. Malar J 12:328. http://dx.doi.org/10.1186/1475-2875-12-328. [PubMed]
25. Makanga B, Yangari P, Rahola N, Rougeron V, Elguero E, Boundenga L, Moukodoum ND, Okouga AP, Arnathau C, Durand P, Willaume E, Ayala D, Fontenille D, Ayala FJ, Renaud F, Ollomo B, Prugnolle F, Paupy C. 2016. Ape malaria transmission and potential for ape-to-human transfers in Africa. Proc Natl Acad Sci U S A 113:5329–5334. http://dx.doi.org/10.1073/pnas.1603008113. [PubMed]
26. Wu L, van den Hoogen LL, Slater H, Walker PG, Ghani AC, Drakeley CJ, Okell LC. 2015. Comparison of diagnostics for the detection of asymptomatic Plasmodium falciparum infections to inform control and elimination strategies. Nature 528:S86–S93. http://dx.doi.org/10.1038/nature16039. [PubMed]
27. Conway DJ. 2007. Molecular epidemiology of malaria. Clin Microbiol Rev 20:188–204. http://dx.doi.org/10.1128/CMR.00021-06. [PubMed]
28. Escalante AA, Ferreira MU, Vinetz JM, Volkman SK, Cui L, Gamboa D, Krogstad DJ, Barry AE, Carlton JM, van Eijk AM, Pradhan K, Mueller I, Greenhouse B, Pacheco MA, Vallejo AF, Herrera S, Felger I. 2015. Malaria molecular epidemiology: lessons from the International Centers of Excellence for Malaria Research Network. Am J Trop Med Hyg 93(Suppl) :79–86. http://dx.doi.org/10.4269/ajtmh.15-0005. [PubMed]
29. Carlton JM, Das A, Escalante AA. 2013. Genomics, population genetics and evolutionary history of Plasmodium vivax. Adv Parasitol 81:203–222. http://dx.doi.org/10.1016/B978-0-12-407826-0.00005-9. [PubMed]
30. Cotter C, Sturrock HJW, Hsiang MS, Liu J, Phillips AA, Hwang J, Gueye CS, Fullman N, Gosling RD, Feachem RGJ. 2013. The changing epidemiology of malaria elimination: new strategies for new challenges. Lancet 382:900–911. http://dx.doi.org/10.1016/S0140-6736(13)60310-4.
31. World Health Organization. 2017. A Framework for Malaria Elimination. World Health Organization, Geneva, Switzerland. https://www.who.int/malaria/publications/atoz/9789241511988/en/.
32. Zimmerman PA, Howes RE. 2015. Malaria diagnosis for malaria elimination. Curr Opin Infect Dis 28:446–454. http://dx.doi.org/10.1097/QCO.0000000000000191. [PubMed]
33. Mukkala AN, Kwan J, Lau R, Harris D, Kain D, Boggild AK. 2018. An update on malaria rapid diagnostic tests. Curr Infect Dis Rep 20:49. http://dx.doi.org/10.1007/s11908-018-0655-4. [PubMed]
34. Kobayashi T, Gamboa D, Ndiaye D, Cui L, Sutton PL, Vinetz JM. 2015. Malaria diagnosis across the international centers of excellence for malaria research: platforms, performance, and standardization. Am J Trop Med Hyg 93(Suppl) :99–109. http://dx.doi.org/10.4269/ajtmh.15-0004. [PubMed]
35. Galatas B, Bassat Q, Mayor A. 2016. Malaria parasites in the asymptomatic: looking for the hay in the haystack. Trends Parasitol 32:296–308. http://dx.doi.org/10.1016/j.pt.2015.11.015. [PubMed]
36. Chen I, Clarke SE, Gosling R, Hamainza B, Killeen G, Magill A, O’Meara W, Price RN, Riley EM. 2016. “Asymptomatic” malaria: a chronic and debilitating infection that should be treated. PLoS Med 13:e1001942. http://dx.doi.org/10.1371/journal.pmed.1001942. [PubMed]
37. Sepúlveda N, Phelan J, Diez-Benavente E, Campino S, Clark TG, Hopkins H, Sutherland C, Drakeley CJ, Beshir KB. 2018. Global analysis of Plasmodium falciparum histidine-rich protein-2 ( pfhrp2) and pfhrp3 gene deletions using whole-genome sequencing data and meta-analysis. Infect Genet Evol 62:211–219. http://dx.doi.org/10.1016/j.meegid.2018.04.039. [PubMed]
38. Gamboa D, Ho MF, Bendezu J, Torres K, Chiodini PL, Barnwell JW, Incardona S, Perkins M, Bell D, McCarthy J, Cheng Q. 2010. A large proportion of P. falciparum isolates in the Amazon region of Peru lack pfhrp2 and pfhrp3: implications for malaria rapid diagnostic tests. PLoS One 5:e8091. http://dx.doi.org/10.1371/journal.pone.0008091. [PubMed]
39. Akinyi S, Hayden T, Gamboa D, Torres K, Bendezu J, Abdallah JF, Griffing SM, Quezada WM, Arrospide N, De Oliveira AM, Lucas C, Magill AJ, Bacon DJ, Barnwell JW, Udhayakumar V. 2013. Multiple genetic origins of histidine-rich protein 2 gene deletion in Plasmodium falciparum parasites from Peru. Sci Rep 3:2797. http://dx.doi.org/10.1038/srep02797. [PubMed]
40. World Health Organization. 2016. P. falciparum hrp2/3 gene deletions. Malaria Policy Advisory Committee Meeting. WHO/HTM/GMP/MPAC/2016.12. http://www.who.int/malaria/mpac/mpac-sept2016-hrp2-consultation-short-report-session7.pdf?ua=1.
41. Bharti PK, Chandel HS, Ahmad A, Krishna S, Udhayakumar V, Singh N. 2016. Prevalence of pfhrp2 and/or pfhrp3 gene deletion in Plasmodium falciparum population in eight highly endemic states in India. PLoS One 11:e0157949. http://dx.doi.org/10.1371/journal.pone.0157949. [PubMed]
42. Patel JC, Oberstaller J, Xayavong M, Narayanan J, DeBarry JD, Srinivasamoorthy G, Villegas L, Escalante AA, DaSilva A, Peterson DS, Barnwell JW, Kissinger JC, Udhayakumar V, Lucchi NW. 2013. Real-time loop-mediated isothermal amplification (RealAmp) for the species-specific identification of Plasmodium vivax. PLoS One 8:e54986. http://dx.doi.org/10.1371/journal.pone.0054986. [PubMed]
43. Hofmann N, Mwingira F, Shekalaghe S, Robinson LJ, Mueller I, Felger I. 2015. Ultra-sensitive detection of Plasmodium falciparum by amplification of multi-copy subtelomeric targets. PLoS Med 12:e1001788. http://dx.doi.org/10.1371/journal.pmed.1001788. [PubMed]
44. Vallejo AF, Martínez NL, González IJ, Arévalo-Herrera M, Herrera S. 2015. Evaluation of the loop mediated isothermal DNA amplification (LAMP) kit for malaria diagnosis in P. vivax endemic settings of Colombia. PLoS Negl Trop Dis 9:e3453. http://dx.doi.org/10.1371/journal.pntd.0003453. [PubMed]
45. Chaumeau V, Kajeechiwa L, Fustec B, Landier J, Naw Nyo S, Nay Hsel S, Phatharakokordbun P, Kittiphanakun P, Nosten S, Thwin MM, Win Tun S, Wiladphaingern J, Cottrell G, Parker DM, Minh MC, Kwansomboon N, Metaane S, Montazeau C, Kunjanwong K, Sawasdichai S, Andolina C, Ling C, Haohankhunnatham W, Christiensen P, Wanyatip S, Konghahong K, Cerqueira D, Imwong M, Dondorp AM, Chareonviriyaphap T, White NJ, Nosten FH, Corbel V. 2019. Contribution of asymptomatic Plasmodium infections to the transmission of malaria in Kayin State, Myanmar. J Infect Dis 219:1499–1509. http://dx.doi.org/10.1093/infdis/jiy686. [PubMed]
46. Sturrock HJ, Hsiang MS, Cohen JM, Smith DL, Greenhouse B, Bousema T, Gosling RD. 2013. Targeting asymptomatic malaria infections: active surveillance in control and elimination. PLoS Med 10:e1001467. http://dx.doi.org/10.1371/journal.pmed.1001467. [PubMed]
47. Slater HC, Ross A, Felger I, Hofmann NE, Robinson L, Cook J, Gonçalves BP, Björkman A, Ouedraogo AL, Morris U, Msellem M, Koepfli C, Mueller I, Tadesse F, Gadisa E, Das S, Domingo G, Kapulu M, Midega J, Owusu-Agyei S, Nabet C, Piarroux R, Doumbo O, Doumbo SN, Koram K, Lucchi N, Udhayakumar V, Mosha J, Tiono A, Chandramohan D, Gosling R, Mwingira F, Sauerwein R, Riley EM, White NJ, Nosten F, Imwong M, Bousema T, Drakeley C, Okell LC. 2019. The temporal dynamics and infectiousness of subpatent Plasmodium falciparum infections in relation to parasite density. Nat Commun 10:1433. http://dx.doi.org/10.1038/s41467-019-09441-1. [PubMed]
48. Sutherland CJ. 2016. Persistent parasitism: the adaptive biology of malariae and ovale malaria. Trends Parasitol 32:808–819. http://dx.doi.org/10.1016/j.pt.2016.07.001. [PubMed]
49. Wampfler R, Mwingira F, Javati S, Robinson L, Betuela I, Siba P, Beck HP, Mueller I, Felger I. 2013. Strategies for detection of Plasmodium species gametocytes. PLoS One 8:e76316. http://dx.doi.org/10.1371/journal.pone.0076316. [PubMed]
50. Koepfli C, Yan G. 2018. Plasmodium gametocytes in field studies: do we measure commitment to transmission or detectability? Trends Parasitol 34:378–387. http://dx.doi.org/10.1016/j.pt.2018.02.009. [PubMed]
51. Imwong M, Stepniewska K, Tripura R, Peto TJ, Lwin KM, Vihokhern B, Wongsaen K, von Seidlein L, Dhorda M, Snounou G, Keereecharoen L, Singhasivanon P, Sirithiranont P, Chalk J, Nguon C, Day NP, Nosten F, Dondorp A, White NJ. 2016. Numerical distributions of parasite densities during asymptomatic malaria. J Infect Dis 213:1322–1329. http://dx.doi.org/10.1093/infdis/jiv596. [PubMed]
52. Molineaux L, Gramiccia G. 1980. The Garki Project: Research on the Epidemiology and Control of Malaria in the Sudan Savanna of West Africa. World Health Organization, Geneva, Switzerland.
53. Dietz K, Molineaux L, Thomas A. 1974. A malaria model tested in the African savannah. Bull World Health Organ 50:347–357.
54. Busula AO, Bousema T, Mweresa CK, Masiga D, Logan JG, Sauerwein RW, Verhulst NO, Takken W, de Boer JG. 2017. Gametocytemia and attractiveness of Plasmodium falciparum-infected Kenyan children to Anopheles gambiae mosquitoes. J Infect Dis 216:291–295. http://dx.doi.org/10.1093/infdis/jix214. [PubMed]
55. Bharti AR, Chuquiyauri R, Brouwer KC, Stancil J, Lin J, Llanos-Cuentas A, Vinetz JM. 2006. Experimental infection of the neotropical malaria vector Anopheles darlingi by human patient-derived Plasmodium vivax in the Peruvian Amazon. Am J Trop Med Hyg 75:610–616. http://dx.doi.org/10.4269/ajtmh.2006.75.610. [PubMed]
56. Lima NF, Bastos MS, Ferreira MU. 2012. Plasmodium vivax: reverse transcriptase real-time PCR for gametocyte detection and quantitation in clinical samples. Exp Parasitol 132:348–354. http://dx.doi.org/10.1016/j.exppara.2012.08.010. [PubMed]
57. Schneider P, Bousema T, Omar S, Gouagna L, Sawa P, Schallig H, Sauerwein R. 2006. (Sub)microscopic Plasmodium falciparum gametocytaemia in Kenyan children after treatment with sulphadoxine-pyrimethamine monotherapy or in combination with artesunate. Int J Parasitol 36:403–408. http://dx.doi.org/10.1016/j.ijpara.2006.01.002. [PubMed]
58. Vallejo AF, García J, Amado-Garavito AB, Arévalo-Herrera M, Herrera S. 2016. Plasmodium vivax gametocyte infectivity in sub-microscopic infections. Malar J 15:48. http://dx.doi.org/10.1186/s12936-016-1104-1. [PubMed]
59. Wampfler R, Timinao L, Beck HP, Soulama I, Tiono AB, Siba P, Mueller I, Felger I. 2014. Novel genotyping tools for investigating transmission dynamics of Plasmodium falciparum. J Infect Dis 210:1188–1197. http://dx.doi.org/10.1093/infdis/jiu236. [PubMed]
60. Bousema T, Okell L, Felger I, Drakeley C. 2014. Asymptomatic malaria infections: detectability, transmissibility and public health relevance. Nat Rev Microbiol 12:833–840. http://dx.doi.org/10.1038/nrmicro3364. [PubMed]
61. Schneider P, Greischar MA, Birget PLG, Repton C, Mideo N, Reece SE. 2018. Adaptive plasticity in the gametocyte conversion rate of malaria parasites. PLoS Pathog 14:e1007371. http://dx.doi.org/10.1371/journal.ppat.1007371. [PubMed]
62. Tadesse FG, Meerstein-Kessel L, Gonçalves BP, Drakeley C, Ranford-Cartwright L, Bousema T. 2019. Gametocyte sex ratio: the key to understanding Plasmodium falciparum transmission? Trends Parasitol 35:226–238. http://dx.doi.org/10.1016/j.pt.2018.12.001. [PubMed]
63. Tibayrenc M, Ayala FJ. 1991. Towards a population genetics of microorganisms: the clonal theory of parasitic protozoa. Parasitol Today 7:228–232. http://dx.doi.org/10.1016/0169-4758(91)90234-F.
64. Charlesworth B. 2009. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205. http://dx.doi.org/10.1038/nrg2526. [PubMed]
65. Chenet SM, Schneider KA, Villegas L, Escalante AA. 2012. Local population structure of Plasmodium: impact on malaria control and elimination. Malar J 11:412. http://dx.doi.org/10.1186/1475-2875-11-412. [PubMed]
66. 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 17:1467–1482. http://dx.doi.org/10.1093/oxfordjournals.molbev.a026247. [PubMed]
67. Anderson TJ, Su XZ, Roddam A, Day KP. 2000. Complex mutations in a high proportion of microsatellite loci from the protozoan parasite Plasmodium falciparum. Mol Ecol 9:1599–1608. http://dx.doi.org/10.1046/j.1365-294x.2000.01057.x. [PubMed]
68. Chenet SM, Taylor JE, Blair S, Zuluaga L, Escalante AA. 2015. Longitudinal analysis of Plasmodium falciparum genetic variation in Turbo, Colombia: implications for malaria control and elimination. Malar J 14:363. http://dx.doi.org/10.1186/s12936-015-0887-9. [PubMed]
69. Roper C, Pearce R, Nair S, Sharp B, Nosten F, Anderson T. 2004. Intercontinental spread of pyrimethamine-resistant malaria. Science 305:1124. http://dx.doi.org/10.1126/science.1098876. [PubMed]
70. Tun KM, Imwong M, Lwin KM, Win AA, Hlaing TM, Hlaing T, Lin K, Kyaw MP, Plewes K, Faiz MA, Dhorda M, Cheah PY, Pukrittayakamee S, Ashley EA, Anderson TJ, Nair S, McDew-White M, Flegg JA, Grist EP, Guerin P, Maude RJ, Smithuis F, Dondorp AM, Day NP, Nosten F, White NJ, Woodrow CJ. 2015. Spread of artemisinin-resistant Plasmodium falciparum in Myanmar: a cross-sectional survey of the K13 molecular marker. Lancet Infect Dis 15:415–421. http://dx.doi.org/10.1016/S1473-3099(15)70032-0.
71. Takala SL, Escalante AA, Branch OH, Kariuki S, Biswas S, Chaiyaroj SC, Lal AA. 2006. Genetic diversity in the block 2 region of the merozoite surface protein 1 (MSP-1) of Plasmodium falciparum: additional complexity and selection and convergence in fragment size polymorphism. Infect Genet Evol 6:417–424. http://dx.doi.org/10.1016/j.meegid.2006.01.009. [PubMed]
72. Haasl RJ, Payseur BA. 2011. Multi-locus inference of population structure: a comparison between single nucleotide polymorphisms and microsatellites. Heredity 106:158–171. http://dx.doi.org/10.1038/hdy.2010.21. [PubMed]
73. Kublin JG, Dzinjalamala FK, Kamwendo DD, Malkin EM, Cortese JF, Martino LM, Mukadam RA, Rogerson SJ, Lescano AG, Molyneux ME, Winstanley PA, Chimpeni P, Taylor TE, Plowe CV. 2002. Molecular markers for failure of sulfadoxine-pyrimethamine and chlorproguanil-dapsone treatment of Plasmodium falciparum malaria. J Infect Dis 185:380–388. http://dx.doi.org/10.1086/338566. [PubMed]
74. Djimdé A, Doumbo OK, Cortese JF, Kayentao K, Doumbo S, Diourté Y, Coulibaly D, Dicko A, Su XZ, Nomura T, Fidock DA, Wellems TE, Plowe CV. 2001. A molecular marker for chloroquine-resistant falciparum malaria. N Engl J Med 344:257–263. http://dx.doi.org/10.1056/NEJM200101253440403. [PubMed]
75. McCollum AM, Poe AC, Hamel M, Huber C, Zhou Z, Shi YP, Ouma P, Vulule J, Bloland P, Slutsker L, Barnwell JW, Udhayakumar V, Escalante AA. 2006. Antifolate resistance in Plasmodium falciparum: multiple origins and identification of novel dhfr alleles. J Infect Dis 194:189–197. http://dx.doi.org/10.1086/504687. [PubMed]
76. Snounou G, Beck HP. 1998. The use of PCR genotyping in the assessment of recrudescence or reinfection after antimalarial drug treatment. Parasitol Today 14:462–467. http://dx.doi.org/10.1016/S0169-4758(98)01340-4.
77. Rice BL, Acosta MM, Pacheco MA, Escalante AA. 2013. Merozoite surface protein-3 alpha as a genetic marker for epidemiologic studies in Plasmodium vivax: a cautionary note. Malar J 12:288. http://dx.doi.org/10.1186/1475-2875-12-288. [PubMed]
78. Mascorro CN, Zhao K, Khuntirat B, Sattabongkot J, Yan G, Escalante AA, Cui L. 2005. Molecular evolution and intragenic recombination of the merozoite surface protein MSP-3alpha from the malaria parasite Plasmodium vivax in Thailand. Parasitology 131:25–35. http://dx.doi.org/10.1017/S0031182005007547. [PubMed]
79. Imwong M, Pukrittayakamee S, Grüner AC, Rénia L, Letourneur F, Looareesuwan S, White NJ, Snounou G. 2005. Practical PCR genotyping protocols for Plasmodium vivax using Pvcs and Pvmsp1. Malar J 4:20. http://dx.doi.org/10.1186/1475-2875-4-20. [PubMed]
80. Mueller I, Schoepflin S, Smith TA, Benton KL, Bretscher MT, Lin E, Kiniboro B, Zimmerman PA, Speed TP, Siba P, Felger I. 2012. Force of infection is key to understanding the epidemiology of Plasmodium falciparum malaria in Papua New Guinean children. Proc Natl Acad Sci U S A 109:10030–10035. http://dx.doi.org/10.1073/pnas.1200841109. [PubMed]
81. Koepfli C, Colborn KL, Kiniboro B, Lin E, Speed TP, Siba PM, Felger I, Mueller I. 2013. A high force of Plasmodium vivax blood-stage infection drives the rapid acquisition of immunity in Papua New Guinean children. PLoS Negl Trop Dis 7:e2403. http://dx.doi.org/10.1371/journal.pntd.0002403. [PubMed]
82. Pacheco MA, Lopez-Perez M, Vallejo AF, Herrera S, Arévalo-Herrera M, Escalante AA. 2016. Multiplicity of infection and disease severity in Plasmodium vivax. PLoS Negl Trop Dis 10:e0004355. http://dx.doi.org/10.1371/journal.pntd.0004355. [PubMed]
83. Pacheco MA, Schneider KA, Céspedes N, Herrera S, Arévalo-Herrera M, Escalante AA. 2019. Limited differentiation among Plasmodium vivax populations from the northwest and to the south Pacific Coast of Colombia: a malaria corridor? PLoS Negl Trop Dis 13:e0007310. http://dx.doi.org/10.1371/journal.pntd.0007310. [PubMed]
84. Koepfli C, Waltmann A, Ome-Kaius M, Robinson LJ, Mueller I. 2018. Multiplicity of infection is a poor predictor of village-Level Plasmodium vivax and P. falciparum population prevalence in the Southwest Pacific. Open Forum Infect Dis 5:ofy240. http://dx.doi.org/10.1093/ofid/ofy240. [PubMed]
85. Karl S, White MT, Milne GJ, Gurarie D, Hay SI, Barry AE, Felger I, Mueller I. 2016. Spatial effects on the multiplicity of Plasmodium falciparum infections. PLoS One 11:e0164054. http://dx.doi.org/10.1371/journal.pone.0164054. [PubMed]
86. Bei AK, Niang M, Deme AB, Daniels RF, Sarr FD, Sokhna C, Talla C, Faye J, Diagne N, Doucoure S, Mboup S, Wirth DF, Tall A, Ndiaye D, Hartl DL, Volkman SK, Toure-Balde A. 2018. Dramatic changes in malaria population genetic complexity in Dielmo and Ndiop, Senegal, revealed using genomic surveillance. J Infect Dis 217:622–627. http://dx.doi.org/10.1093/infdis/jix580. [PubMed]
87. Mobegi VA, Loua KM, Ahouidi AD, Satoguina J, Nwakanma DC, Amambua-Ngwa A, Conway DJ. 2012. Population genetic structure of Plasmodium falciparum across a region of diverse endemicity in West Africa. Malar J 11:223. http://dx.doi.org/10.1186/1475-2875-11-223. [PubMed]
88. Larrañaga N, Mejía RE, Hormaza JI, Montoya A, Soto A, Fontecha GA. 2013. Genetic structure of Plasmodium falciparum populations across the Honduras-Nicaragua border. Malar J 12:354. http://dx.doi.org/10.1186/1475-2875-12-354. [PubMed]
89. Anthony TG, Conway DJ, Cox-Singh J, Matusop A, Ratnam S, Shamsul S, Singh B. 2005. Fragmented population structure of plasmodium falciparum in a region of declining endemicity. J Infect Dis 191:1558–1564. http://dx.doi.org/10.1086/429338. [PubMed]
90. Friedrich LR, Popovici J, Kim S, Dysoley L, Zimmerman PA, Menard D, Serre D. 2016. Complexity of infection and genetic diversity in Cambodian Plasmodium vivax. PLoS Negl Trop Dis 10:e0004526. http://dx.doi.org/10.1371/journal.pntd.0004526. [PubMed]
91. Zhong D, Koepfli C, Cui L, Yan G. 2018. Molecular approaches to determine the multiplicity of Plasmodium infections. Malar J 17:172. http://dx.doi.org/10.1186/s12936-018-2322-5. [PubMed]
92. Arnott A, Wapling J, Mueller I, Ramsland PA, Siba PM, Reeder JC, Barry AE. 2014. Distinct patterns of diversity, population structure and evolution in the AMA1 genes of sympatric Plasmodium falciparum and Plasmodium vivax populations of Papua New Guinea from an area of similarly high transmission. Malar J 13:233. http://dx.doi.org/10.1186/1475-2875-13-233. [PubMed]
93. Chenet SM, Branch OH, Escalante AA, Lucas CM, Bacon DJ. 2008. Genetic diversity of vaccine candidate antigens in Plasmodium falciparum isolates from the Amazon basin of Peru. Malar J 7:93. http://dx.doi.org/10.1186/1475-2875-7-93. [PubMed]
94. Escalante AA, Cornejo OE, Rojas A, Udhayakumar V, Lal AA. 2004. Assessing the effect of natural selection in malaria parasites. Trends Parasitol 20:388–395. http://dx.doi.org/10.1016/j.pt.2004.06.002. [PubMed]
95. Takala SL, Coulibaly D, Thera MA, Batchelor AH, Cummings MP, Escalante AA, Ouattara A, Traoré K, Niangaly A, Djimdé AA, Doumbo OK, Plowe CV. 2009. Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci Transl Med 1:2ra5. http://dx.doi.org/10.1126/scitranslmed.3000257. [PubMed]
96. Hartl DL. 2004. The origin of malaria: mixed messages from genetic diversity. Nat Rev Microbiol 2:15–22. http://dx.doi.org/10.1038/nrmicro795. [PubMed]
97. Joy DA, Feng X, Mu J, Furuya T, Chotivanich K, Krettli AU, Ho M, Wang A, White NJ, Suh E, Beerli P, Su XZ. 2003. Early origin and recent expansion of Plasmodium falciparum. Science 300:318–321. http://dx.doi.org/10.1126/science.1081449. [PubMed]
98. Taylor JE, Pacheco MA, Bacon DJ, Beg MA, Machado RL, Fairhurst RM, Herrera S, Kim JY, Menard D, Póvoa MM, Villegas L, Mulyanto, Snounou G, 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 30:2050–2064. http://dx.doi.org/10.1093/molbev/mst104. [PubMed]
99. Cornejo OE, Escalante AA. 2006. The origin and age of Plasmodium vivax. Trends Parasitol 22:558–563. http://dx.doi.org/10.1016/j.pt.2006.09.007. [PubMed]
100. 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 20:1283–1289. http://dx.doi.org/10.1016/j.cub.2010.05.053. [PubMed]
101. Rodrigues PT, Valdivia HO, de Oliveira TC, Alves JMP, 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. Sci Rep 8:1993. http://dx.doi.org/10.1038/s41598-018-19554-0. [PubMed]
102. Tessema SK, Monk SL, Schultz MB, Tavul L, Reeder JC, Siba PM, Mueller I, Barry AE. 2015. Phylogeography of var gene repertoires reveals fine-scale geospatial clustering of Plasmodium falciparum populations in a highly endemic area. Mol Ecol 24:484–497. http://dx.doi.org/10.1111/mec.13033. [PubMed]
103. Cui L, Escalante AA, Imwong M, Snounou G. 2003. The genetic diversity of Plasmodium vivax populations. Trends Parasitol 19:220–226. http://dx.doi.org/10.1016/S1471-4922(03)00085-0.
104. Pacheco MA, Poe AC, Collins WE, Lal AA, Tanabe K, Kariuki SK, Udhayakumar V, Escalante AA. 2007. A comparative study of the genetic diversity of the 42kDa fragment of the merozoite surface protein 1 in Plasmodium falciparum and P. vivax. Infect Genet Evol 7:180–187. http://dx.doi.org/10.1016/j.meegid.2006.08.002. [PubMed]
105. Pacheco MA, Elango AP, Rahman AA, Fisher D, Collins WE, Barnwell JW, Escalante AA. 2012. Evidence of purifying selection on merozoite surface protein 8 (MSP8) and 10 (MSP10) in Plasmodium spp. Infect Genet Evol 12:978–986. http://dx.doi.org/10.1016/j.meegid.2012.02.009. [PubMed]
106. Lin JT, Hathaway NJ, Saunders DL, Lon C, Balasubramanian S, Kharabora O, Gosi P, Sriwichai S, Kartchner L, Chuor CM, Satharath P, Lanteri C, Bailey JA, Juliano JJ. 2015. Using amplicon deep sequencing to detect genetic signatures of Plasmodium vivax relapse. J Infect Dis 212:999–1008. http://dx.doi.org/10.1093/infdis/jiv142. [PubMed]
107. Neafsey DE, et al. 2015. Genetic diversity and protective efficacy of the RTS,S/AS01 malaria vaccine. N Engl J Med 373:2025–2037. http://dx.doi.org/10.1056/NEJMoa1505819. [PubMed]
108. Rao PN, Uplekar S, Kayal S, Mallick PK, Bandyopadhyay N, Kale S, Singh OP, Mohanty A, Mohanty S, Wassmer SC, Carlton JM. 2016. A method for amplicon deep sequencing of drug resistance genes in Plasmodium falciparum clinical isolates from India. J Clin Microbiol 54:1500–1511. http://dx.doi.org/10.1128/JCM.00235-16. [PubMed]
109. Talundzic E, Ravishankar S, Kelley J, Patel D, Plucinski M, Schmedes S, Ljolje D, Clemons B, Madison-Antenucci S, Arguin PM, Lucchi NW, Vannberg F, Udhayakumar V. 2018. Next-generation sequencing and bioinformatics protocol for malaria drug resistance marker surveillance. Antimicrob Agents Chemother 62:e02474-17. http://dx.doi.org/10.1128/AAC.02474-17. [PubMed]
110. Pacheco MA, Kadakia ER, Chaudhary Z, Perkins DJ, Kelley J, Ravishankar S, Cranfield M, Talundzic E, Udhayakumar V, Escalante AA. 2019. Evolution and genetic diversity of the k13 gene associated with artemisinin delayed parasite clearance in Plasmodium falciparum. Antimicrob Agents Chemother 63:e02550-18. http://dx.doi.org/10.1128/AAC.02550-18. [PubMed]
111. Orjuela-Sánchez P, Sá JM, Brandi MC, Rodrigues PT, Bastos MS, Amaratunga C, Duong S, Fairhurst RM, Ferreira MU. 2013. Higher microsatellite diversity in Plasmodium vivax than in sympatric Plasmodium falciparum populations in Pursat, Western Cambodia. Exp Parasitol 134:318–326. http://dx.doi.org/10.1016/j.exppara.2013.03.029. [PubMed]
112. Sutton PL. 2013. A call to arms: on refining Plasmodium vivax microsatellite marker panels for comparing global diversity. Malar J 12:447. http://dx.doi.org/10.1186/1475-2875-12-447. [PubMed]
113. Daniels R, Volkman SK, Milner DA, Mahesh N, Neafsey DE, Park DJ, Rosen D, Angelino E, Sabeti PC, Wirth DF, Wiegand RC. 2008. A general SNP-based molecular barcode for Plasmodium falciparum identification and tracking. Malar J 7:223. http://dx.doi.org/10.1186/1475-2875-7-223. [PubMed]
114. Baniecki ML, Faust AL, Schaffner SF, Park DJ, Galinsky K, Daniels RF, Hamilton E, Ferreira MU, Karunaweera ND, Serre D, Zimmerman PA, Sá JM, Wellems TE, Musset L, Legrand E, Melnikov A, Neafsey DE, Volkman SK, Wirth DF, Sabeti PC. 2015. Development of a single nucleotide polymorphism barcode to genotype Plasmodium vivax infections. PLoS Negl Trop Dis 9:e0003539. http://dx.doi.org/10.1371/journal.pntd.0003539. [PubMed]
115. Alifrangis M, Nag S, Schousboe ML, Ishengoma D, Lusingu J, Pota H, Kavishe RA, Pearce R, Ord R, Lynch C, Dejene S, Cox J, Rwakimari J, Minja DT, Lemnge MM, Roper C. 2014. Independent origin of Plasmodium falciparum antifolate super-resistance, Uganda, Tanzania, and Ethiopia. Emerg Infect Dis 20:1280–1286. http://dx.doi.org/10.3201/eid2008.131897. [PubMed]
116. Cheeseman IH, Miller BA, Nair S, Nkhoma S, Tan A, Tan JC, Al Saai S, Phyo AP, Moo CL, Lwin KM, McGready R, Ashley E, Imwong M, Stepniewska K, Yi P, Dondorp AM, Mayxay M, Newton PN, White NJ, Nosten F, Ferdig MT, Anderson TJ. 2012. A major genome region underlying artemisinin resistance in malaria. Science 336:79–82. http://dx.doi.org/10.1126/science.1215966. [PubMed]
117. McCollum AM, Schneider KA, Griffing SM, Zhou Z, Kariuki S, Ter-Kuile F, Shi YP, Slutsker L, Lal AA, Udhayakumar V, Escalante AA. 2012. Differences in selective pressure on dhps and dhfr drug resistant mutations in western Kenya. Malar J 11:77. http://dx.doi.org/10.1186/1475-2875-11-77. [PubMed]
118. Schultz L, Wapling J, Mueller I, Ntsuke PO, Senn N, Nale J, Kiniboro B, Buckee CO, Tavul L, Siba PM, Reeder JC, Barry AE. 2010. Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission. Malar J 9:336. http://dx.doi.org/10.1186/1475-2875-9-336. [PubMed]
119. Waltmann A, Koepfli C, Tessier N, Karl S, Fola A, Darcy AW, Wini L, Harrison GLA, Barnadas C, Jennison C, Karunajeewa H, Boyd S, Whittaker M, Kazura J, Bahlo M, Mueller I, Barry AE. 2018. Increasingly inbred and fragmented populations of Plasmodium vivax associated with the eastward decline in malaria transmission across the Southwest Pacific. PLoS Negl Trop Dis 12:e0006146. http://dx.doi.org/10.1371/journal.pntd.0006146. [PubMed]
120. Gunawardena S, Ferreira MU, Kapilananda GM, Wirth DF, Karunaweera ND. 2014. The Sri Lankan paradox: high genetic diversity in Plasmodium vivax populations despite decreasing levels of malaria transmission. Parasitology 141:880–890. http://dx.doi.org/10.1017/S0031182013002278. [PubMed]
121. Koepfli C, Timinao L, Antao T, Barry AE, Siba P, Mueller I, Felger I. 2013. A large Plasmodium vivax reservoir and little population structure in the South Pacific. PLoS One 8:e66041. http://dx.doi.org/10.1371/journal.pone.0066041. [PubMed]
122. Smith JM, Haigh J. 1974. The hitch-hiking effect of a favourable gene. Genet Res 23:23–35. http://dx.doi.org/10.1017/S0016672300014634.
123. Kim Y, Stephan W. 2002. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160:765–777.
124. Wootton JC, Feng X, Ferdig MT, Cooper RA, Mu J, Baruch DI, Magill AJ, Su XZ. 2002. Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418:320–323. http://dx.doi.org/10.1038/nature00813. [PubMed]
125. Nair S, Williams JT, Brockman A, Paiphun L, Mayxay M, Newton PN, Guthmann JP, Smithuis FM, Hien TT, White NJ, Nosten F, Anderson TJ. 2003. A selective sweep driven by pyrimethamine treatment in Southeast Asian malaria parasites. Mol Biol Evol 20:1526–1536. http://dx.doi.org/10.1093/molbev/msg162. [PubMed]
126. Lachance J, Tishkoff SA. 2013. SNP ascertainment bias in population genetic analyses: why it is important, and how to correct it. Bioessays 35:780–786. http://dx.doi.org/10.1002/bies.201300014. [PubMed]
127. Sisya TJ, Kamn’gona RM, Vareta JA, Fulakeza JM, Mukaka MF, Seydel KB, Laufer MK, Taylor TE, Nkhoma SC. 2015. Subtle changes in Plasmodium falciparum infection complexity following enhanced intervention in Malawi. Acta Trop 142:108–114. http://dx.doi.org/10.1016/j.actatropica.2014.11.008. [PubMed]
128. Daniels R, Chang HH, Séne PD, Park DC, Neafsey DE, Schaffner SF, Hamilton EJ, Lukens AK, Van Tyne D, Mboup S, Sabeti PC, Ndiaye D, Wirth DF, Hartl DL, Volkman SK. 2013. Genetic surveillance detects both clonal and epidemic transmission of malaria following enhanced intervention in Senegal. PLoS One 8:e60780. http://dx.doi.org/10.1371/journal.pone.0060780. [PubMed]
129. Popovici J, Pierce-Friedrich L, Kim S, Bin S, Run V, Lek D, Hee KHD, Lee Soon-U L, Cannon MV, Serre D, Menard D. 2019. Recrudescence, reinfection, or relapse? A more rigorous framework to assess chloroquine efficacy for Plasmodium vivax malaria. J Infect Dis 219:315–322. http://dx.doi.org/10.1093/infdis/jiy484. [PubMed]
130. Obaldia N3rd, Baro NK, Calzada JE, Santamaria AM, Daniels R, Wong W, Chang HH, Hamilton EJ, Arevalo-Herrera M, Herrera S, Wirth DF, Hartl DL, Marti M, Volkman SK. 2015. Clonal outbreak of Plasmodium falciparum infection in eastern Panama. J Infect Dis 211:1087–1096. [PubMed]
131. Nkhoma SC, Nair S, Al-Saai S, Ashley E, McGready R, Phyo AP, Nosten F, Anderson TJ. 2013. Population genetic correlates of declining transmission in a human pathogen. Mol Ecol 22:273–285. http://dx.doi.org/10.1111/mec.12099. [PubMed]
132. Auburn S, Barry AE. 2017. Dissecting malaria biology and epidemiology using population genetics and genomics. Int J Parasitol 47:77–85. http://dx.doi.org/10.1016/j.ijpara.2016.08.006. [PubMed]
133. Auburn S, Marfurt J, Maslen G, Campino S, Ruano Rubio V, Manske M, Machunter B, Kenangalem E, Noviyanti R, Trianty L, Sebayang B, Wirjanata G, Sriprawat K, Alcock D, Macinnis B, Miotto O, Clark TG, Russell B, Anstey NM, Nosten F, Kwiatkowski DP, Price RN. 2013. Effective preparation of Plasmodium vivax field isolates for high-throughput whole genome sequencing. PLoS One 8:e53160. http://dx.doi.org/10.1371/journal.pone.0053160. [PubMed]
134. Oyola SO, Gu Y, Manske M, Otto TD, O’Brien J, Alcock D, Macinnis B, Berriman M, Newbold CI, Kwiatkowski DP, Swerdlow HP, Quail MA. 2013. Efficient depletion of host DNA contamination in malaria clinical sequencing. J Clin Microbiol 51:745–751. http://dx.doi.org/10.1128/JCM.02507-12. [PubMed]
135. Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Lwin KM, Ariey F, Hanpithakpong W, Lee SJ, Ringwald P, Silamut K, Imwong M, Chotivanich K, Lim P, Herdman T, An SS, Yeung S, Singhasivanon P, Day NP, Lindegardh N, Socheat D, White NJ. 2009. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med 361:455–467. http://dx.doi.org/10.1056/NEJMoa0808859. [PubMed]
136. Takala-Harrison S, Clark TG, Jacob CG, Cummings MP, Miotto O, Dondorp AM, Fukuda MM, Nosten F, Noedl H, Imwong M, Bethell D, Se Y, Lon C, Tyner SD, Saunders DL, Socheat D, Ariey F, Phyo AP, Starzengruber P, Fuehrer HP, Swoboda P, Stepniewska K, Flegg J, Arze C, Cerqueira GC, Silva JC, Ricklefs SM, Porcella SF, Stephens RM, Adams M, Kenefic LJ, Campino S, Auburn S, MacInnis B, Kwiatkowski DP, Su XZ, White NJ, Ringwald P, Plowe CV. 2013. Genetic loci associated with delayed clearance of Plasmodium falciparum following artemisinin treatment in Southeast Asia. Proc Natl Acad Sci U S A 110:240–245. http://dx.doi.org/10.1073/pnas.1211205110. [PubMed]
137. Miotto O, Amato R, Ashley EA, MacInnis B, Almagro-Garcia J, Amaratunga C, Lim P, Mead D, Oyola SO, Dhorda M, Imwong M, Woodrow C, Manske M, Stalker J, Drury E, Campino S, Amenga-Etego L, Thanh TN, Tran HT, Ringwald P, Bethell D, Nosten F, Phyo AP, Pukrittayakamee S, Chotivanich K, Chuor CM, Nguon C, Suon S, Sreng S, Newton PN, Mayxay M, Khanthavong M, Hongvanthong B, Htut Y, Han KT, Kyaw MP, Faiz MA, Fanello CI, Onyamboko M, Mokuolu OA, Jacob CG, Takala-Harrison S, Plowe CV, Day NP, Dondorp AM, Spencer CC, McVean G, Fairhurst RM, White NJ, Kwiatkowski DP. 2015. Genetic architecture of artemisinin-resistant Plasmodium falciparum. Nat Genet 47:226–234. http://dx.doi.org/10.1038/ng.3189. [PubMed]
138. Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois AC, Khim N, Kim S, Duru V, Bouchier C, Ma L, Lim P, Leang R, Duong S, Sreng S, Suon S, Chuor CM, Bout DM, Ménard S, Rogers WO, Genton B, Fandeur T, Miotto O, Ringwald P, Le Bras J, Berry A, Barale JC, Fairhurst RM, Benoit-Vical F, Mercereau-Puijalon O, Ménard D. 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature 505:50–55. http://dx.doi.org/10.1038/nature12876. [PubMed]
139. Amato R, Lim P, Miotto O, Amaratunga C, Dek D, Pearson RD, Almagro-Garcia J, Neal AT, Sreng S, Suon S, Drury E, Jyothi D, Stalker J, Kwiatkowski DP, Fairhurst RM. 2017. Genetic markers associated with dihydroartemisinin-piperaquine failure in Plasmodium falciparum malaria in Cambodia: a genotype-phenotype association study. Lancet Infect Dis 17:164–173. http://dx.doi.org/10.1016/S1473-3099(16)30409-1.
140. Neafsey DE, Galinsky K, Jiang RH, Young L, Sykes SM, Saif S, Gujja S, Goldberg JM, Young S, Zeng Q, Chapman SB, Dash AP, Anvikar AR, Sutton PL, Birren BW, Escalante AA, Barnwell JW, Carlton JM. 2012. The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat Genet 44:1046–1050. http://dx.doi.org/10.1038/ng.2373. [PubMed]
141. Winter DJ, Pacheco MA, Vallejo AF, Schwartz RS, Arevalo-Herrera M, Herrera S, Cartwright RA, Escalante AA. 2015. Whole genome sequencing of field isolates reveals extensive genetic diversity in Plasmodium vivax from Colombia. PLoS Negl Trop Dis 9:e0004252. http://dx.doi.org/10.1371/journal.pntd.0004252. [PubMed]
142. Hupalo DN, Luo Z, Melnikov A, Sutton PL, Rogov P, Escalante A, Vallejo AF, Herrera S, Arévalo-Herrera M, Fan Q, Wang Y, Cui L, Lucas CM, Durand S, Sanchez JF, Baldeviano GC, Lescano AG, Laman M, Barnadas C, Barry A, Mueller I, Kazura JW, Eapen A, Kanagaraj D, Valecha N, Ferreira MU, Roobsoong W, Nguitragool W, Sattabonkot J, Gamboa D, Kosek M, Vinetz JM, González-Cerón L, Birren BW, Neafsey DE, Carlton JM. 2016. Population genomics studies identify signatures of global dispersal and drug resistance in Plasmodium vivax. Nat Genet 48:953–958. http://dx.doi.org/10.1038/ng.3588. [PubMed]
143. Amambua-Ngwa A, Tetteh KK, Manske M, Gomez-Escobar N, Stewart LB, Deerhake ME, Cheeseman IH, Newbold CI, Holder AA, Knuepfer E, Janha O, Jallow M, Campino S, Macinnis B, Kwiatkowski DP, Conway DJ. 2012. Population genomic scan for candidate signatures of balancing selection to guide antigen characterization in malaria parasites. PLoS Genet 8:e1002992. http://dx.doi.org/10.1371/journal.pgen.1002992. [PubMed]
144. Mobegi VA, Duffy CW, Amambua-Ngwa A, Loua KM, Laman E, Nwakanma DC, MacInnis B, Aspeling-Jones H, Murray L, Clark TG, Kwiatkowski DP, Conway DJ. 2014. Genome-wide analysis of selection on the malaria parasite Plasmodium falciparum in West African populations of differing infection endemicity. Mol Biol Evol 31:1490–1499. http://dx.doi.org/10.1093/molbev/msu106. [PubMed]
145. Henden L, Lee S, Mueller I, Barry A, Bahlo M. 2018. Identity-by-descent analyses for measuring population dynamics and selection in recombining pathogens. PLoS Genet 14:e1007279. http://dx.doi.org/10.1371/journal.pgen.1007279. [PubMed]
146. Schaffner SF, Taylor AR, Wong W, Wirth DF, Neafsey DE. 2018. hmmIBD: software to infer pairwise identity by descent between haploid genotypes. Malar J 17:196. http://dx.doi.org/10.1186/s12936-018-2349-7. [PubMed]
147. Taylor AR, Schaffner SF, Cerqueira GC, Nkhoma SC, Anderson TJC, Sriprawat K, Pyae Phyo A, Nosten F, Neafsey DE, Buckee CO. 2017. Quantifying connectivity between local Plasmodium falciparum malaria parasite populations using identity by descent. PLoS Genet 13:e1007065. http://dx.doi.org/10.1371/journal.pgen.1007065. [PubMed]
148. Cornejo OE, Fisher D, Escalante AA. 2014. Genome-wide patterns of genetic polymorphism and signatures of selection in Plasmodium vivax. Genome Biol Evol 7:106–119. http://dx.doi.org/10.1093/gbe/evu267. [PubMed]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.AME-0010-2019
2019-08-09
2019-08-19

Abstract:

Malaria is a vector-borne disease that involves multiple parasite species in a variety of ecological settings. However, the parasite species causing the disease, the prevalence of subclinical infections, the emergence of drug resistance, the scale-up of interventions, and the ecological factors affecting malaria transmission, among others, are aspects that vary across areas where malaria is endemic. Such complexities have propelled the study of parasite genetic diversity patterns in the context of epidemiologic investigations. Importantly, molecular studies indicate that the time and spatial distribution of malaria cases reflect epidemiologic processes that cannot be fully understood without characterizing the evolutionary forces shaping parasite population genetic patterns. Although broad in scope, this review in the Curated Collection: Advances in Molecular Epidemiology highlights the need for understanding population genetic concepts when interpreting parasite molecular data. First, we discuss malaria complexity in terms of the parasite species involved. Second, we describe how molecular data are changing our understanding of malaria incidence and infectiousness. Third, we compare different approaches to generate parasite genetic information in the context of epidemiologically relevant questions related to malaria control. Finally, we describe a few genomic studies as evidence of how these approaches will provide new insights into the malaria disease dynamics.

*This article is part of a curated collection.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of FIGURE 1
FIGURE 1

Phylogeny of parasites based on the mitochondrial genome. The phylogenetic tree shows all the species parasitic to humans, including those that cause zoonotic malarias. Although not a comprehensive phylogeny, it evidences that parasites causing human malaria are not a monophyletic group.

Source: microbiolspec August 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.AME-0010-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2
FIGURE 2

life cycle. The haplontic life cycle comprises a vertebrate host and a dipteran vector. In human malarias, an infected female mosquito inoculates haploid sporozoites into the host. These sporozoites invade the liver cells and mature into schizonts. The schizonts rupture, releasing merozoites that infect the red blood cells. Some species develop dormant liver stages or hypnozoites that can produce merozoites at a later time (relapse). A fraction of merozoites differentiates into gametocytes (micro- and macrogametocytes). All these stages are haploid. These gametocytes are then taken up by an mosquito, in which zygote formation takes place (diploid stage). Due to the nature of the cycle, inbreeding is common. The zygote differentiates into ookinetes and oocysts, the latter with a syncytial cell or sporoblast containing thousands of nuclei in which meiosis takes place, producing haploid sporozoites.

Source: microbiolspec August 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.AME-0010-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 3
FIGURE 3

Approaches in malaria molecular epidemiology. Shown are techniques and approaches commonly used to generate molecular information in the context of epidemiologic investigations.

Source: microbiolspec August 2019 vol. 7 no. 4 doi:10.1128/microbiolspec.AME-0010-2019
Permissions and Reprints Request Permissions
Download as Powerpoint

Supplemental Material

No supplementary material available for this content.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error