Skip to main content
Top
Published in: Malaria Journal 1/2011

Open Access 01-12-2011 | Research

Sexual recombination is a signature of a persisting malaria epidemic in Peru

Authors: Patrick L Sutton, Lindsay P Torres, OraLee H Branch

Published in: Malaria Journal | Issue 1/2011

Login to get access

Abstract

Background

The aim of this study was to consider the impact that multi-clone, complex infections have on a parasite population structure in a low transmission setting. In general, complexity of infection (minimum number of clones within an infection) and the overall population level diversity is expected to be minimal in low transmission settings. Additionally, the parasite population structure is predicted to be clonal, rather than sexual due to infrequent parasite inoculation and lack of recombination between genetically distinct clones. However, in this low transmission of the Peruvian Amazon, complex infections are becoming more frequent, in spite of decreasing infection prevalence. In this study, it was hypothesized that sexual recombination between distinct clonal lineages of Plasmodium falciparum parasites were altering the subpopulation structure and effectively maintaining the population-level diversity.

Methods

Fourteen microsatellite markers were chosen to describe the genetic diversity in 313 naturally occurring P. falciparum infections from Peruvian Amazon. The population and subpopulation structure was characterized by measuring: clusteredness, expected heterozygosity (He), allelic richness, private allelic richness, and linkage disequilibrium. Next, microsatellite haplotypes and alleles were correlated with P. falciparum merozoite surface protein 1 Block 2 (Pf msp1-B2) to examine the presence of recombinant microsatellite haplotypes.

Results

The parasite population structure consists of six genetically diverse subpopulations of clones, called "clusters". Clusters 1, 3, 4, and 6 have unique haplotypes that exceed 70% of the total number of clones within each cluster, while Clusters 2 and 5 have a lower proportion of unique haplotypes, but still exceed 46%. By measuring the He, allelic richness, and private allelic richness within each of the six subpopulations, relatively low levels of genetic diversity within each subpopulation (except Cluster 4) are observed. This indicated that the number of alleles, and not the combination of alleles, are limited. Next, the standard index of association (IAS) was measured, which revealed a significant decay in linkage disequilibrium (LD) associated with Cluster 6, which is indicative of independent assortment of alleles. This decay in LD is a signature of this subpopulation approaching linkage equilibrium by undergoing sexual recombination. To trace possible recombination events, the two most frequent microsatellite haplotypes observed over time (defined by either a K1 or Mad20) were selected as the progenitors and then potential recombinants were identified in within the natural population.

Conclusions

Contrary to conventional low transmission models, this study provides evidence of a parasite population structure that is superficially defined by a clonal backbone. Sexual recombination does occur and even arguably is responsible for maintaining the substructure of this population.
Appendix
Available only for authorised users
Literature
1.
go back to reference 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: Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol. 2000, 17: 1467-1482.CrossRefPubMed 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: Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Mol Biol Evol. 2000, 17: 1467-1482.CrossRefPubMed
2.
go back to reference Barker GC: Microsatellite DNA: a tool for population genetic analysis. Trans R Soc Trop Med Hyg. 2002, 96: S21-S24.CrossRefPubMed Barker GC: Microsatellite DNA: a tool for population genetic analysis. Trans R Soc Trop Med Hyg. 2002, 96: S21-S24.CrossRefPubMed
3.
go back to reference Su X-Z, Wellems TE: Toward a high-resolution Plasmodium falciparum linkage map: polymorphic markers from hundreds of simple sequence repeats. Genomics. 1996, 33: 430-444. 10.1006/geno.1996.0218.CrossRefPubMed Su X-Z, Wellems TE: Toward a high-resolution Plasmodium falciparum linkage map: polymorphic markers from hundreds of simple sequence repeats. Genomics. 1996, 33: 430-444. 10.1006/geno.1996.0218.CrossRefPubMed
4.
go back to reference Havryliuk T, Ferreira MU: A closer look at multiple-clone Plasmodium vivax infections: detection methods, prevalence and consequences. Mem Inst Oswaldo Cruz. 2009, 104: 67-73.CrossRefPubMed Havryliuk T, Ferreira MU: A closer look at multiple-clone Plasmodium vivax infections: detection methods, prevalence and consequences. Mem Inst Oswaldo Cruz. 2009, 104: 67-73.CrossRefPubMed
5.
go back to reference Imwong M, Sudimack D, Pukrittayakamee S, Osorio L, Carlton JM, Day NP, White NJ, Anderson TJ: Microsatellite variation, repeat array length, and population history of Plasmodium vivax. Mol Biol Evol. 2006, 23: 1016-1018. 10.1093/molbev/msj116.CrossRefPubMed Imwong M, Sudimack D, Pukrittayakamee S, Osorio L, Carlton JM, Day NP, White NJ, Anderson TJ: Microsatellite variation, repeat array length, and population history of Plasmodium vivax. Mol Biol Evol. 2006, 23: 1016-1018. 10.1093/molbev/msj116.CrossRefPubMed
6.
go back to reference Cooper A, Tait A, Sweeney L, Tweedie A, Morrison L, Turner CM, MacLeod A: Genetic analysis of the human infective trypanosome Trypanosoma brucei gambiense: chromosomal segregation, crossing over, and the construction of a genetic map. Genome Biol. 2008, 9: R103-10.1186/gb-2008-9-6-r103.PubMedCentralCrossRefPubMed Cooper A, Tait A, Sweeney L, Tweedie A, Morrison L, Turner CM, MacLeod A: Genetic analysis of the human infective trypanosome Trypanosoma brucei gambiense: chromosomal segregation, crossing over, and the construction of a genetic map. Genome Biol. 2008, 9: R103-10.1186/gb-2008-9-6-r103.PubMedCentralCrossRefPubMed
7.
go back to reference Ajzenberg D, Bañuls AL, Tibayrenc M, Dardé ML: Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. Int J Parasitol. 2002, 32: 27-38. 10.1016/S0020-7519(01)00301-0.CrossRefPubMed Ajzenberg D, Bañuls AL, Tibayrenc M, Dardé ML: Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups. Int J Parasitol. 2002, 32: 27-38. 10.1016/S0020-7519(01)00301-0.CrossRefPubMed
8.
go back to reference Schwenkenbecher JM, Wirth T, Schnur LF, Jaffe CL, Schallig H, Al-Jawabreh A, Hamarsheh O, Azmi K, Pratlong F, Schönian G: Microsatellite analysis reveals genetic structure of Leishmania tropica. Int J Parasitol. 2006, 36: 237-246. 10.1016/j.ijpara.2005.09.010.CrossRefPubMed Schwenkenbecher JM, Wirth T, Schnur LF, Jaffe CL, Schallig H, Al-Jawabreh A, Hamarsheh O, Azmi K, Pratlong F, Schönian G: Microsatellite analysis reveals genetic structure of Leishmania tropica. Int J Parasitol. 2006, 36: 237-246. 10.1016/j.ijpara.2005.09.010.CrossRefPubMed
9.
go back to reference Oliveira RP, Broude NE, Macedo AM, Cantor CR, Smith CL, Pena SD: Probing the genetic population structure of Trypanosoma cruzi with polymorphic microsatellites. Proc Natl Acad Sci USA. 1998, 95: 3776-3780. 10.1073/pnas.95.7.3776.PubMedCentralCrossRefPubMed Oliveira RP, Broude NE, Macedo AM, Cantor CR, Smith CL, Pena SD: Probing the genetic population structure of Trypanosoma cruzi with polymorphic microsatellites. Proc Natl Acad Sci USA. 1998, 95: 3776-3780. 10.1073/pnas.95.7.3776.PubMedCentralCrossRefPubMed
10.
go back to reference Simo G, Njiokou F, Tume C, Lueong S, De Meeûs T, Cuny G, Asonganyi T: Population genetic structure of Central African Trypanosoma brucei gambiense isolates using microsatellite DNA markers. Infect Genet Evol. 2010, 10: 68-76. 10.1016/j.meegid.2009.09.019.CrossRefPubMed Simo G, Njiokou F, Tume C, Lueong S, De Meeûs T, Cuny G, Asonganyi T: Population genetic structure of Central African Trypanosoma brucei gambiense isolates using microsatellite DNA markers. Infect Genet Evol. 2010, 10: 68-76. 10.1016/j.meegid.2009.09.019.CrossRefPubMed
11.
go back to reference Imwong M, Nair S, Pukrittayakamee S, Sudimack D, Williams JT, Mayxay M, Newton PN, Kim JR, Nandy A, Osorio L, Carlton JM, White NJ, Day NP, Anderson TJ: Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. Int J Parasitol. 2007, 37: 1013-1022. 10.1016/j.ijpara.2007.02.010.CrossRefPubMed Imwong M, Nair S, Pukrittayakamee S, Sudimack D, Williams JT, Mayxay M, Newton PN, Kim JR, Nandy A, Osorio L, Carlton JM, White NJ, Day NP, Anderson TJ: Contrasting genetic structure in Plasmodium vivax populations from Asia and South America. Int J Parasitol. 2007, 37: 1013-1022. 10.1016/j.ijpara.2007.02.010.CrossRefPubMed
12.
go back to reference Conrad M, Zubacova Z, Dunn LA, Upcroft J, Sullivan SA, Tachezy J, Carlton JM: Microsatellite polymorphism in the sexually transmitted human pathogen Trichomonas vaginalis indicates a genetically diverse parasite. Mol Biochem Parasitol. 2011, 175: 30-38. 10.1016/j.molbiopara.2010.08.006.PubMedCentralCrossRefPubMed Conrad M, Zubacova Z, Dunn LA, Upcroft J, Sullivan SA, Tachezy J, Carlton JM: Microsatellite polymorphism in the sexually transmitted human pathogen Trichomonas vaginalis indicates a genetically diverse parasite. Mol Biochem Parasitol. 2011, 175: 30-38. 10.1016/j.molbiopara.2010.08.006.PubMedCentralCrossRefPubMed
13.
go back to reference Rich SM, Hudson RR, Ayala FJ: Plasmodium falciparum antigenic diversity: evidence of clonal population structure. Proc Natl Acad Sci USA. 1997, 94: 13040-13045. 10.1073/pnas.94.24.13040.PubMedCentralCrossRefPubMed Rich SM, Hudson RR, Ayala FJ: Plasmodium falciparum antigenic diversity: evidence of clonal population structure. Proc Natl Acad Sci USA. 1997, 94: 13040-13045. 10.1073/pnas.94.24.13040.PubMedCentralCrossRefPubMed
14.
go back to reference Rich SM, Licht MC, Hudson RR, Ayala FJ: Malaria's eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc Natl Acad Sci USA. 1998, 95: 4425-4430. 10.1073/pnas.95.8.4425.PubMedCentralCrossRefPubMed Rich SM, Licht MC, Hudson RR, Ayala FJ: Malaria's eve: evidence of a recent population bottleneck throughout the world populations of Plasmodium falciparum. Proc Natl Acad Sci USA. 1998, 95: 4425-4430. 10.1073/pnas.95.8.4425.PubMedCentralCrossRefPubMed
15.
go back to reference Coluzzi M: The clay feet of the malaria giant and its African roots: hypotheses and inferences about origin, spread and control of Plasmodium falciparum. Parassitologia. 1999, 41: 277-283.PubMed Coluzzi M: The clay feet of the malaria giant and its African roots: hypotheses and inferences about origin, spread and control of Plasmodium falciparum. Parassitologia. 1999, 41: 277-283.PubMed
16.
go back to reference Volkman SK, Barry AE, Lyons EJ, Nielsen KM, Thomas SM, Choi M, Thakore SS, Day KP, Wirth DF, Hartl DL: Recent origin of Plasmodium falciparum from a single progenitor. Science. 2001, 293: 482-484. 10.1126/science.1059878.CrossRefPubMed Volkman SK, Barry AE, Lyons EJ, Nielsen KM, Thomas SM, Choi M, Thakore SS, Day KP, Wirth DF, Hartl DL: Recent origin of Plasmodium falciparum from a single progenitor. Science. 2001, 293: 482-484. 10.1126/science.1059878.CrossRefPubMed
17.
go back to reference Tibayrenc M, Kjellberg F, Arnaud J, Oury B, Brenière SF, Dardé ML, Ayala FJ: Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc Natl Acad Sci USA. 1991, 88: 5129-5133. 10.1073/pnas.88.12.5129.PubMedCentralCrossRefPubMed Tibayrenc M, Kjellberg F, Arnaud J, Oury B, Brenière SF, Dardé ML, Ayala FJ: Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc Natl Acad Sci USA. 1991, 88: 5129-5133. 10.1073/pnas.88.12.5129.PubMedCentralCrossRefPubMed
18.
go back to reference Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P, Teuscher T, Walliker D: Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology. 1994, 109: 413-421. 10.1017/S0031182000080665.CrossRefPubMed Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P, Teuscher T, Walliker D: Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology. 1994, 109: 413-421. 10.1017/S0031182000080665.CrossRefPubMed
19.
go back to reference Su X-Z, Ferdig MT, Huang Y, Huynh CQ, Liu A, You J, Wootton JC, Wellems TE: A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Science. 1999, 286: 1351-1353. 10.1126/science.286.5443.1351.CrossRefPubMed Su X-Z, Ferdig MT, Huang Y, Huynh CQ, Liu A, You J, Wootton JC, Wellems TE: A genetic map and recombination parameters of the human malaria parasite Plasmodium falciparum. Science. 1999, 286: 1351-1353. 10.1126/science.286.5443.1351.CrossRefPubMed
20.
go back to reference Conway DJ, Roper C, Oduola AM, Arnot DE, Kremsner PG, Grobusch MP, Curtis CF, Greenwood BM: High recombination rate in natural populations of Plasmodium falciparum. Proc Natl Acad Sci USA. 1999, 96: 4506-4511. 10.1073/pnas.96.8.4506.PubMedCentralCrossRefPubMed Conway DJ, Roper C, Oduola AM, Arnot DE, Kremsner PG, Grobusch MP, Curtis CF, Greenwood BM: High recombination rate in natural populations of Plasmodium falciparum. Proc Natl Acad Sci USA. 1999, 96: 4506-4511. 10.1073/pnas.96.8.4506.PubMedCentralCrossRefPubMed
21.
go back to reference Hey J: Parasite populations: the puzzle of Plasmodium. Curr Biol. 1999, 9: R565-R567. 10.1016/S0960-9822(99)80356-X.CrossRefPubMed Hey J: Parasite populations: the puzzle of Plasmodium. Curr Biol. 1999, 9: R565-R567. 10.1016/S0960-9822(99)80356-X.CrossRefPubMed
22.
go back to reference Mu J, Duan J, Makova K, Joy DA, Huynh CQ, Branch OH, Li W-H, Su X-Z: Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature. 2001, 418: 323-326.CrossRef Mu J, Duan J, Makova K, Joy DA, Huynh CQ, Branch OH, Li W-H, Su X-Z: Chromosome-wide SNPs reveal an ancient origin for Plasmodium falciparum. Nature. 2001, 418: 323-326.CrossRef
23.
go back to reference Hughes AL, Verra F: Very large long-term effective population size in the virulent human malaria parasite Plasmodium falciparum. Proc R Soc London B Biol Sci. 2001, 268: 1855-1860. 10.1098/rspb.2001.1759.CrossRef Hughes AL, Verra F: Very large long-term effective population size in the virulent human malaria parasite Plasmodium falciparum. Proc R Soc London B Biol Sci. 2001, 268: 1855-1860. 10.1098/rspb.2001.1759.CrossRef
24.
go back to reference Joy DA, Feng X, Mu J, Furuya T, Chotivanich K, Krettli AU, Ho M, Wang A, White NJ, Suh E, Beerly P, Su X-Z: Early origin and recent expansion of Plasmodium falciparum. Science. 2003, 300: 318-321. 10.1126/science.1081449.CrossRefPubMed Joy DA, Feng X, Mu J, Furuya T, Chotivanich K, Krettli AU, Ho M, Wang A, White NJ, Suh E, Beerly P, Su X-Z: Early origin and recent expansion of Plasmodium falciparum. Science. 2003, 300: 318-321. 10.1126/science.1081449.CrossRefPubMed
25.
go back to reference Tibayrenc M, Ayala FJ: The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol. 2002, 18: 405-10. 10.1016/S1471-4922(02)02357-7.CrossRefPubMed Tibayrenc M, Ayala FJ: The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol. 2002, 18: 405-10. 10.1016/S1471-4922(02)02357-7.CrossRefPubMed
26.
go back to reference Mzilahowa T, McCall PJ, Hastings IM: "Sexual" population structure and genetics of the malaria agent P. falciparum. PLoS One. 2007, 18: 2- Mzilahowa T, McCall PJ, Hastings IM: "Sexual" population structure and genetics of the malaria agent P. falciparum. PLoS One. 2007, 18: 2-
27.
go back to reference Razakandrainibe FG, Durand P, Koella JC, De Meeus T, Rousset F, Ayala FJ, Renaud F: "Clonal" population structure of the malaria agent Plasmodium falciparum in high-infection regions. Proc Natl Acad Sci USA. 2005, 102: 17388-17393. 10.1073/pnas.0508871102.PubMedCentralCrossRefPubMed Razakandrainibe FG, Durand P, Koella JC, De Meeus T, Rousset F, Ayala FJ, Renaud F: "Clonal" population structure of the malaria agent Plasmodium falciparum in high-infection regions. Proc Natl Acad Sci USA. 2005, 102: 17388-17393. 10.1073/pnas.0508871102.PubMedCentralCrossRefPubMed
28.
go back to reference Anderson TJC, Paul REL, Donnelly CA, Day KP: Do malaria parasites mate non-randomly within the mosquito mid gut?. Genet Res. 2000, 75: 285-296. 10.1017/S0016672300004481.CrossRefPubMed Anderson TJC, Paul REL, Donnelly CA, Day KP: Do malaria parasites mate non-randomly within the mosquito mid gut?. Genet Res. 2000, 75: 285-296. 10.1017/S0016672300004481.CrossRefPubMed
29.
go back to reference Prugnolle F, De Meeus T: Apparent high recombination rates in clonal parasitic organisms due to inappropriate sampling design. Heredity. 2010, 104: 135-40. 10.1038/hdy.2009.128.CrossRefPubMed Prugnolle F, De Meeus T: Apparent high recombination rates in clonal parasitic organisms due to inappropriate sampling design. Heredity. 2010, 104: 135-40. 10.1038/hdy.2009.128.CrossRefPubMed
30.
go back to reference Conway DJ, McBride JS: Population genetics of Plasmodium falciparum within a malaria hyperendemic area. Parasitology. 1991, 103: 7-16. 10.1017/S0031182000059229.CrossRefPubMed Conway DJ, McBride JS: Population genetics of Plasmodium falciparum within a malaria hyperendemic area. Parasitology. 1991, 103: 7-16. 10.1017/S0031182000059229.CrossRefPubMed
31.
go back to reference Sinden RE, Hartley RH: Identification of the meiotic division of malarial parasites. J Protozool. 1985, 32: 742-744.CrossRefPubMed Sinden RE, Hartley RH: Identification of the meiotic division of malarial parasites. J Protozool. 1985, 32: 742-744.CrossRefPubMed
32.
go back to reference Sinden RE, Hartley RH, Winger L: The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of meiotic division. Parasitology. 1985, 91 (Pt 2): 227-244.CrossRefPubMed Sinden RE, Hartley RH, Winger L: The development of Plasmodium ookinetes in vitro: an ultrastructural study including a description of meiotic division. Parasitology. 1985, 91 (Pt 2): 227-244.CrossRefPubMed
33.
go back to reference Walliker D, Quakyi IA, Wellems TE, McCutchan TF, Szarfman A, London WT, Corcoran LM, Burkot TR, Carter R: Genetic analysis of the human malaria parasite Plasmodium falciparum. Science. 1987, 236: 1661-1666. 10.1126/science.3299700.CrossRefPubMed Walliker D, Quakyi IA, Wellems TE, McCutchan TF, Szarfman A, London WT, Corcoran LM, Burkot TR, Carter R: Genetic analysis of the human malaria parasite Plasmodium falciparum. Science. 1987, 236: 1661-1666. 10.1126/science.3299700.CrossRefPubMed
34.
go back to reference Hill W, Babiker H: Estimation of numbers of malaria clones in blood samples. Proc R Soc Lond B. 1995, 262: 249-257. 10.1098/rspb.1995.0203.CrossRef Hill W, Babiker H: Estimation of numbers of malaria clones in blood samples. Proc R Soc Lond B. 1995, 262: 249-257. 10.1098/rspb.1995.0203.CrossRef
35.
go back to reference Branch O, Takala S, Kariuki S, Nahlen B, Kolczak M, Hawley W, Lal A: Plasmodium falciparum genotypes, low complexity of infection, and resistance to subsequent malaria in participants in the Asembo Bay Cohort Project. Infect Immun. 2001, 69: 7783-7792. 10.1128/IAI.69.12.7783-7792.2001.PubMedCentralCrossRefPubMed Branch O, Takala S, Kariuki S, Nahlen B, Kolczak M, Hawley W, Lal A: Plasmodium falciparum genotypes, low complexity of infection, and resistance to subsequent malaria in participants in the Asembo Bay Cohort Project. Infect Immun. 2001, 69: 7783-7792. 10.1128/IAI.69.12.7783-7792.2001.PubMedCentralCrossRefPubMed
36.
go back to reference Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker S, Smith DL, Moyeed RA, Snow RW: A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 2009, 6: e1000048-PubMedCentralCrossRefPubMed Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, Noor AM, Kabaria CW, Manh BH, Elyazar IR, Brooker S, Smith DL, Moyeed RA, Snow RW: A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med. 2009, 6: e1000048-PubMedCentralCrossRefPubMed
37.
go back to reference Konate L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, Spiegel A, Trape JF, Mercereau-Puijalon O: Variation of Plasmodium falciparum msp1 block 2 and msp2 allele prevalence and of infection complexity in two neighbouring Senegalese villages with different transmission conditions. Trans R Soc Trop Med Hyg. 1999, 93: 21-28.CrossRefPubMed Konate L, Zwetyenga J, Rogier C, Bischoff E, Fontenille D, Tall A, Spiegel A, Trape JF, Mercereau-Puijalon O: Variation of Plasmodium falciparum msp1 block 2 and msp2 allele prevalence and of infection complexity in two neighbouring Senegalese villages with different transmission conditions. Trans R Soc Trop Med Hyg. 1999, 93: 21-28.CrossRefPubMed
38.
go back to reference Paul REL, Day KP: Mating Patterns of Plasmodium falciparum. Parasitol Today. 1998, 14: 197-202. 10.1016/S0169-4758(98)01226-5.CrossRefPubMed Paul REL, Day KP: Mating Patterns of Plasmodium falciparum. Parasitol Today. 1998, 14: 197-202. 10.1016/S0169-4758(98)01226-5.CrossRefPubMed
39.
go back to reference Paul REL, Hackford I, Brockman A, Muller-Graf C, Price R, Luxemburger C, White NJ, Nosten F, Day KP: Transmission intensity and Plasmodium falciparum diversity on the northwestern border of Thailand. Am J Trop Med Hyg. 1998, 58: 195-203.PubMed Paul REL, Hackford I, Brockman A, Muller-Graf C, Price R, Luxemburger C, White NJ, Nosten F, Day KP: Transmission intensity and Plasmodium falciparum diversity on the northwestern border of Thailand. Am J Trop Med Hyg. 1998, 58: 195-203.PubMed
40.
go back to reference Robert F, Ntoumi F, Angel G, Candito D, Rogier C, Fandeur T, Sarthou JL, Mercereau-Puijalon O: Extensive genetic diversity of Plasmodium falciparum isolates collected from patients with severe malaria in Dakar, Senegal. Trans R Soc Trop Med Hyg. 1996, 90: 704-711. 10.1016/S0035-9203(96)90446-0.CrossRefPubMed Robert F, Ntoumi F, Angel G, Candito D, Rogier C, Fandeur T, Sarthou JL, Mercereau-Puijalon O: Extensive genetic diversity of Plasmodium falciparum isolates collected from patients with severe malaria in Dakar, Senegal. Trans R Soc Trop Med Hyg. 1996, 90: 704-711. 10.1016/S0035-9203(96)90446-0.CrossRefPubMed
41.
go back to reference Sutton PL, Neyra V, Hernandez JN, Branch OH: Plasmodium falciparum and Plasmodium vivax infections in the Peruvian Amazon: propagation of complex, multiple allele-type infections without superinfection. Am J Trop Med Hyg. 2009, 81: 950-960. 10.4269/ajtmh.2009.09-0132.PubMedCentralCrossRefPubMed Sutton PL, Neyra V, Hernandez JN, Branch OH: Plasmodium falciparum and Plasmodium vivax infections in the Peruvian Amazon: propagation of complex, multiple allele-type infections without superinfection. Am J Trop Med Hyg. 2009, 81: 950-960. 10.4269/ajtmh.2009.09-0132.PubMedCentralCrossRefPubMed
42.
go back to reference Urdaneta L, Lal A, Barnabe C, Oury B, Goldman I, Ayala FJ, Tibayrenc M: Evidence for clonal propagation in natural isolates of Plasmodium falciparum from Venezuela. Proc Natl Acad Sci USA. 2001, 98: 6725-6729. 10.1073/pnas.111144998.PubMedCentralCrossRefPubMed Urdaneta L, Lal A, Barnabe C, Oury B, Goldman I, Ayala FJ, Tibayrenc M: Evidence for clonal propagation in natural isolates of Plasmodium falciparum from Venezuela. Proc Natl Acad Sci USA. 2001, 98: 6725-6729. 10.1073/pnas.111144998.PubMedCentralCrossRefPubMed
43.
go back to reference Jordan SJ, Branch OH, Castro JC, Oster RA, Rayner JC: Genetic diversity of the malaria vaccine candidate Plasmodium falciparum merozoite surface protein-3 in a hypoendemic transmission environment. Am J Trop Med Hyg. 2009, 80: 479-486.PubMedCentralPubMed Jordan SJ, Branch OH, Castro JC, Oster RA, Rayner JC: Genetic diversity of the malaria vaccine candidate Plasmodium falciparum merozoite surface protein-3 in a hypoendemic transmission environment. Am J Trop Med Hyg. 2009, 80: 479-486.PubMedCentralPubMed
44.
go back to reference Sutton PL, Clark EH, Silva C, Branch OH: The Plasmodium falciparum merozoite surface protein-1 19 KD antibody response in the Peruvian Amazon predominantly targets the non-allele specific, shared sites of this antigen. Malar J. 2010, 9: 3-10.1186/1475-2875-9-3.PubMedCentralCrossRefPubMed Sutton PL, Clark EH, Silva C, Branch OH: The Plasmodium falciparum merozoite surface protein-1 19 KD antibody response in the Peruvian Amazon predominantly targets the non-allele specific, shared sites of this antigen. Malar J. 2010, 9: 3-10.1186/1475-2875-9-3.PubMedCentralCrossRefPubMed
45.
go back to reference Neal AT, Jordan SJ, Oliveira AL, Hernandez JN, Branch OH, Rayner JC: Limited variation in vaccine candidate Plasmodium falciparum Merozoite Surface Protein-6 over multiple transmission seasons. Malar J. 2010, 9: 138-10.1186/1475-2875-9-138.PubMedCentralCrossRefPubMed Neal AT, Jordan SJ, Oliveira AL, Hernandez JN, Branch OH, Rayner JC: Limited variation in vaccine candidate Plasmodium falciparum Merozoite Surface Protein-6 over multiple transmission seasons. Malar J. 2010, 9: 138-10.1186/1475-2875-9-138.PubMedCentralCrossRefPubMed
46.
go back to reference Branch OH, Sutton PL, Barnes CR, Castro JC, Hussin J, Awadalla P, Guerra GH: Plasmodium falciparum genetic diversity maintained and amplified over five years of a low transmission endemic in the Peruvian Amazon. Mol Biol Evol. 2010, 28: 1973-1986.PubMedCentralCrossRefPubMed Branch OH, Sutton PL, Barnes CR, Castro JC, Hussin J, Awadalla P, Guerra GH: Plasmodium falciparum genetic diversity maintained and amplified over five years of a low transmission endemic in the Peruvian Amazon. Mol Biol Evol. 2010, 28: 1973-1986.PubMedCentralCrossRefPubMed
47.
go back to reference Branch O, Casapia WM, Gamboa DV, Hernandez JN, Alava FF, Roncal N, Alvarez E, Perez EJ, Gotuzzo E: Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malaria infections in a recently emerged, hypoendemic Peruvian Amazon community. Malar J. 2005, 4: 27-10.1186/1475-2875-4-27.PubMedCentralCrossRefPubMed Branch O, Casapia WM, Gamboa DV, Hernandez JN, Alava FF, Roncal N, Alvarez E, Perez EJ, Gotuzzo E: Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malaria infections in a recently emerged, hypoendemic Peruvian Amazon community. Malar J. 2005, 4: 27-10.1186/1475-2875-4-27.PubMedCentralCrossRefPubMed
48.
go back to reference Rubio JM, Benito A, Roche J, Berzosa PJ, Garcia ML, Mico M, Edu M, Alvar J: Semi-nested, multiplex polymerase chain reaction for detection of human malaria parasites and evidence of Plasmodium vivax infection in Equatorial Guinea. Am J Trop Med Hyg. 1999, 60: 183-187.PubMed Rubio JM, Benito A, Roche J, Berzosa PJ, Garcia ML, Mico M, Edu M, Alvar J: Semi-nested, multiplex polymerase chain reaction for detection of human malaria parasites and evidence of Plasmodium vivax infection in Equatorial Guinea. Am J Trop Med Hyg. 1999, 60: 183-187.PubMed
49.
go back to reference Takala S, Branch O, Escalante AA, Kariuki S, Wootton J, Lal AA: Evidence for intragenic recombination in Plasmodium falciparum: identification of a novel allele family in block 2 of merozoite surface protein-1: Asembo Bay Area Cohort Project XIV. Mol Biochem Parasitol. 2002, 125: 163-171. 10.1016/S0166-6851(02)00237-2.PubMedCentralCrossRefPubMed Takala S, Branch O, Escalante AA, Kariuki S, Wootton J, Lal AA: Evidence for intragenic recombination in Plasmodium falciparum: identification of a novel allele family in block 2 of merozoite surface protein-1: Asembo Bay Area Cohort Project XIV. Mol Biochem Parasitol. 2002, 125: 163-171. 10.1016/S0166-6851(02)00237-2.PubMedCentralCrossRefPubMed
50.
go back to reference Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics. 2000, 155: 945-959.PubMedCentralPubMed Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics. 2000, 155: 945-959.PubMedCentralPubMed
51.
go back to reference Rosenberg NA, Mahajan S, Ramachandran S, Zhao C, Pritchard JK, Feldman MW: Clines, clusters, and the effect of study design on the inference of human population structure. PLoS Genet. 2005, 1: e70-10.1371/journal.pgen.0010070.PubMedCentralCrossRefPubMed Rosenberg NA, Mahajan S, Ramachandran S, Zhao C, Pritchard JK, Feldman MW: Clines, clusters, and the effect of study design on the inference of human population structure. PLoS Genet. 2005, 1: e70-10.1371/journal.pgen.0010070.PubMedCentralCrossRefPubMed
52.
go back to reference Excoffier L, Valval G, Schneider S: Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online. 2005, 1: 47-50.PubMedCentral Excoffier L, Valval G, Schneider S: Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online. 2005, 1: 47-50.PubMedCentral
53.
go back to reference Polzin T, Daneschmand S: On Steiner trees and minimum spanning trees in hypergraphs. Operations research Letters. 2003, 31: 12-20. 10.1016/S0167-6377(02)00185-2.CrossRef Polzin T, Daneschmand S: On Steiner trees and minimum spanning trees in hypergraphs. Operations research Letters. 2003, 31: 12-20. 10.1016/S0167-6377(02)00185-2.CrossRef
54.
go back to reference Haubold H, Hudson RR: LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics. 2000, 16: 847-848. 10.1093/bioinformatics/16.9.847.CrossRefPubMed Haubold H, Hudson RR: LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics. 2000, 16: 847-848. 10.1093/bioinformatics/16.9.847.CrossRefPubMed
55.
go back to reference Szpiech ZA, Jakobsson M, Rosenberg NA: ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics. 2008, 24: 2498-2504. 10.1093/bioinformatics/btn478.PubMedCentralCrossRefPubMed Szpiech ZA, Jakobsson M, Rosenberg NA: ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics. 2008, 24: 2498-2504. 10.1093/bioinformatics/btn478.PubMedCentralCrossRefPubMed
56.
go back to reference Taylor LH, Read AF: Determinants of transmission success of individual clones from mixed-clone infections of the rodent malaria parasite, Plasmodium chabaudi. Int J Parasitol. 1998, 28: 719-725. 10.1016/S0020-7519(98)00032-0.CrossRefPubMed Taylor LH, Read AF: Determinants of transmission success of individual clones from mixed-clone infections of the rodent malaria parasite, Plasmodium chabaudi. Int J Parasitol. 1998, 28: 719-725. 10.1016/S0020-7519(98)00032-0.CrossRefPubMed
57.
go back to reference Taylor LH, Walliker D, Read AF: Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitol. 1997, 115: 121-132. 10.1017/S0031182097001145.CrossRef Taylor LH, Walliker D, Read AF: Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitol. 1997, 115: 121-132. 10.1017/S0031182097001145.CrossRef
58.
go back to reference De Roode JC, Pansini R, Cheesman SJ, Helinski MEH, Huijben S, Wargo AW, Bell AS, Chan BHK, Walliker D, Read AF: Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci USA. 2005, 102: 7624-7628. 10.1073/pnas.0500078102.PubMedCentralCrossRefPubMed De Roode JC, Pansini R, Cheesman SJ, Helinski MEH, Huijben S, Wargo AW, Bell AS, Chan BHK, Walliker D, Read AF: Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci USA. 2005, 102: 7624-7628. 10.1073/pnas.0500078102.PubMedCentralCrossRefPubMed
59.
go back to reference Wargo AR, de Roode JC, Huijben S, Drew DR, Read AF: Transmission stage investment of malaria parasites in response to in-host competition. Proc R Soc Biol. 2007, 274: 2629-2538. 10.1098/rspb.2007.0873.CrossRef Wargo AR, de Roode JC, Huijben S, Drew DR, Read AF: Transmission stage investment of malaria parasites in response to in-host competition. Proc R Soc Biol. 2007, 274: 2629-2538. 10.1098/rspb.2007.0873.CrossRef
60.
go back to reference Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GAT: The epidemiology of Plasmodium falciparum gametocytes: weapons of mass destruction. Trends Parasitol. 2006, 22: 424-430. 10.1016/j.pt.2006.07.001.CrossRefPubMed Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GAT: The epidemiology of Plasmodium falciparum gametocytes: weapons of mass destruction. Trends Parasitol. 2006, 22: 424-430. 10.1016/j.pt.2006.07.001.CrossRefPubMed
61.
go back to reference Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsuk S, Tosukhowong T, Vannaphan S, Gay F, Mazier D, Looareesuwan S: Decreased hemoglobin concentration, hyperparasitemia, and severe malaria are associated with increased Plasmodium falciparum gametocyte carriage. J Parasitol. 2002, 88: 97-101.CrossRefPubMed Nacher M, Singhasivanon P, Silachamroon U, Treeprasertsuk S, Tosukhowong T, Vannaphan S, Gay F, Mazier D, Looareesuwan S: Decreased hemoglobin concentration, hyperparasitemia, and severe malaria are associated with increased Plasmodium falciparum gametocyte carriage. J Parasitol. 2002, 88: 97-101.CrossRefPubMed
62.
go back to reference Paul REL, Lafond T, Mϋller-Graf CDM, Nithiuthai S, Brey PT, Koella JC: Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections. Evol Biol. 2004, 4: 30-10.1186/1471-2148-4-30. Paul REL, Lafond T, Mϋller-Graf CDM, Nithiuthai S, Brey PT, Koella JC: Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections. Evol Biol. 2004, 4: 30-10.1186/1471-2148-4-30.
63.
go back to reference Reece SE, Duncan AB, West SA, Read AF: Host cell preference and variable transmission strategies in malaria parasites. Proc R Soc B. 2005, 272: 511-517. 10.1098/rspb.2004.2972.PubMedCentralCrossRefPubMed Reece SE, Duncan AB, West SA, Read AF: Host cell preference and variable transmission strategies in malaria parasites. Proc R Soc B. 2005, 272: 511-517. 10.1098/rspb.2004.2972.PubMedCentralCrossRefPubMed
64.
go back to reference Prugnolle F, Durand P, Jacob K, Razakandrainibe F, Arnathau C, Villarreal D, Rousset F, de Meeûs T, Renaud F: A comparison of Anopheles gambiae and Plasmodium falciparum genetic structure over space and time. Microb Infect. 2008, 10: 269-275. 10.1016/j.micinf.2007.12.021.CrossRef Prugnolle F, Durand P, Jacob K, Razakandrainibe F, Arnathau C, Villarreal D, Rousset F, de Meeûs T, Renaud F: A comparison of Anopheles gambiae and Plasmodium falciparum genetic structure over space and time. Microb Infect. 2008, 10: 269-275. 10.1016/j.micinf.2007.12.021.CrossRef
65.
go back to reference Hughes A: Positive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum. Mol Biol Evol. 1992, 9: 381-393.PubMed Hughes A: Positive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum. Mol Biol Evol. 1992, 9: 381-393.PubMed
66.
go back to reference Gupta S, Day KP: A strain theory of malaria transmission. Parasitol Today. 1994, 10: 476-481. 10.1016/0169-4758(94)90160-0.CrossRefPubMed Gupta S, Day KP: A strain theory of malaria transmission. Parasitol Today. 1994, 10: 476-481. 10.1016/0169-4758(94)90160-0.CrossRefPubMed
67.
go back to reference Kouyos RD, Silander OK, Bonhoeffer S: Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol Evol. 2007, 22: 308-315. 10.1016/j.tree.2007.02.014.CrossRefPubMed Kouyos RD, Silander OK, Bonhoeffer S: Epistasis between deleterious mutations and the evolution of recombination. Trends Ecol Evol. 2007, 22: 308-315. 10.1016/j.tree.2007.02.014.CrossRefPubMed
68.
go back to reference Hill WG, Robertson A: The effect of linkage on limits to artificial selection. Genetical Res. 1966, 8: 269-294. 10.1017/S0016672300010156.CrossRef Hill WG, Robertson A: The effect of linkage on limits to artificial selection. Genetical Res. 1966, 8: 269-294. 10.1017/S0016672300010156.CrossRef
69.
go back to reference Eshel I, Feldman MW: On the evolutionary effect of recombination. Theor Popul Biol. 1970, 1: 88-100. 10.1016/0040-5809(70)90043-2.CrossRefPubMed Eshel I, Feldman MW: On the evolutionary effect of recombination. Theor Popul Biol. 1970, 1: 88-100. 10.1016/0040-5809(70)90043-2.CrossRefPubMed
70.
go back to reference Feldman MW, Otto SP, Christiansen FB: Population genetic perspectives on the evolution of recombination. Annu Rev Genet. 1996, 30: 261-295. 10.1146/annurev.genet.30.1.261.CrossRefPubMed Feldman MW, Otto SP, Christiansen FB: Population genetic perspectives on the evolution of recombination. Annu Rev Genet. 1996, 30: 261-295. 10.1146/annurev.genet.30.1.261.CrossRefPubMed
71.
go back to reference Rathod PK, McErlean T, Lee PC: Variations in frequencies of drug resistance in Plasmodium falciparum. Proc Natl Acad Sci USA. 1997, 94: 9389-9393. 10.1073/pnas.94.17.9389.PubMedCentralCrossRefPubMed Rathod PK, McErlean T, Lee PC: Variations in frequencies of drug resistance in Plasmodium falciparum. Proc Natl Acad Sci USA. 1997, 94: 9389-9393. 10.1073/pnas.94.17.9389.PubMedCentralCrossRefPubMed
72.
go back to reference Hill AV, Yates SN, Allsopp CE, Gupta S, Gilbert SC, Lalvani A, Aidoo M, Davenport M, Plebanski M: Human leukocyte antigens and natural selection by malaria. Philos Trans R Soc Lond B Biol Sci. 1994, 346: 379-385. 10.1098/rstb.1994.0155.CrossRefPubMed Hill AV, Yates SN, Allsopp CE, Gupta S, Gilbert SC, Lalvani A, Aidoo M, Davenport M, Plebanski M: Human leukocyte antigens and natural selection by malaria. Philos Trans R Soc Lond B Biol Sci. 1994, 346: 379-385. 10.1098/rstb.1994.0155.CrossRefPubMed
73.
go back to reference Ali E, Mackinnon MJ, Abdel-Muhsin AA, Ahmed S, Walliker D, Babiker HA: Increased density but not prevalence of gametocytes following drug treatment of Plasmodium falciparum. Trans R Soc Trop Med Hyg. 2006, 100: 176-183. 10.1016/j.trstmh.2005.04.021.CrossRefPubMed Ali E, Mackinnon MJ, Abdel-Muhsin AA, Ahmed S, Walliker D, Babiker HA: Increased density but not prevalence of gametocytes following drug treatment of Plasmodium falciparum. Trans R Soc Trop Med Hyg. 2006, 100: 176-183. 10.1016/j.trstmh.2005.04.021.CrossRefPubMed
Metadata
Title
Sexual recombination is a signature of a persisting malaria epidemic in Peru
Authors
Patrick L Sutton
Lindsay P Torres
OraLee H Branch
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2011
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-10-329

Other articles of this Issue 1/2011

Malaria Journal 1/2011 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.