Skip to main content
Top
Published in: Malaria Journal 1/2010

Open Access 01-12-2010 | Research

Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission

Authors: Lee Schultz, Johanna Wapling, Ivo Mueller, Pilate O Ntsuke, Nicolas Senn, Joe Nale, Benson Kiniboro, Caroline O Buckee, Livingstone Tavul, Peter M Siba, John C Reeder, Alyssa E Barry

Published in: Malaria Journal | Issue 1/2010

Login to get access

Abstract

Background

The South West Pacific nation of Papua New Guinea has intense year round transmission of Plasmodium falciparum on the coast and in the low-lying inland areas. Local heterogeneity in the epidemiology of malaria suggests that parasites from multiple locations will need to be surveyed to define the population biology of P. falciparum in the region. This study describes the population genetics of P. falciparum in thirteen villages spread over four distinct catchment areas of Papua New Guinea.

Methods

Ten microsatellite loci were genotyped in 318 P. falciparum isolates from the parasite populations of two inland catchment areas, namely Wosera (number of villages (n) = 7) and Utu (n = 1) and; and two coastal catchments, Malala (n = 3) and Mugil (n = 3). Analysis of the resultant multilocus haplotypes was done at different spatial scales (2-336 km) to define the genetic diversity (allelic richness and expected heterozygosity), linkage disequilibrium and population structure throughout the study area.

Results

Although genetic diversity was high in all parasite populations, it was also variable with a lower allelic richness and expected heterozygosity for inland populations compared to those from the more accessible coast. This variability was not correlated with two proxy measures of transmission intensity, the infection prevalence and the proportion multiple infections. Random associations among the microsatellite loci were observed in all four catchments showing that a substantial degree of out-crossing occurs in the region. Moderate to very high levels of population structure were found but the amount of genetic differentiation (F ST ) did not correlate with geographic distance suggesting that parasite populations are fragmented. Population structure was also identified between villages within the Malala area, with the haplotypes of one parasite population clustering with the neighbouring catchment of Mugil.

Conclusion

The observed population genetics of P. falciparum in this region is likely to be a consequence of the high transmission intensity combined with the isolation of human and vector populations, especially those located inland and migration of parasites via human movement into coastal populations. The variable genetic diversity and population structure of P. falciparum has important implications for malaria control strategies and warrants further fine scale sampling throughout Papua New Guinea.
Appendix
Available only for authorised users
Literature
1.
go back to reference Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI: The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005, 434: 214-217. 10.1038/nature03342.PubMedCentralCrossRefPubMed Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI: The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005, 434: 214-217. 10.1038/nature03342.PubMedCentralCrossRefPubMed
2.
go back to reference Anderson TJ, 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 TJ, 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
3.
go back to reference Mu J, Awadalla P, Duan J, McGee KM, Joy DA, McVean GA, Su XZ: Recombination hotspots and population structure in Plasmodium falciparum. PLoS Biol. 2005, 3: e335-10.1371/journal.pbio.0030335.PubMedCentralCrossRefPubMed Mu J, Awadalla P, Duan J, McGee KM, Joy DA, McVean GA, Su XZ: Recombination hotspots and population structure in Plasmodium falciparum. PLoS Biol. 2005, 3: e335-10.1371/journal.pbio.0030335.PubMedCentralCrossRefPubMed
4.
go back to reference Machado RL, Povoa MM, Calvosa VS, Ferreira MU, Rossit AR, dos Santos EJ, Conway DJ: Genetic structure of Plasmodium falciparum populations in the Brazilian Amazon region. J Infect Dis. 2004, 190: 1547-1555. 10.1086/424601.CrossRefPubMed Machado RL, Povoa MM, Calvosa VS, Ferreira MU, Rossit AR, dos Santos EJ, Conway DJ: Genetic structure of Plasmodium falciparum populations in the Brazilian Amazon region. J Infect Dis. 2004, 190: 1547-1555. 10.1086/424601.CrossRefPubMed
5.
go back to reference Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, Sitthi-Amorn C, Renaud F, Harnyuttanakorn P: Genetic diversity and population structure of Plasmodium falciparum in Thailand, a low transmission country. Malar J. 2009, 8: 155-10.1186/1475-2875-8-155.PubMedCentralCrossRefPubMed Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, Sitthi-Amorn C, Renaud F, Harnyuttanakorn P: Genetic diversity and population structure of Plasmodium falciparum in Thailand, a low transmission country. Malar J. 2009, 8: 155-10.1186/1475-2875-8-155.PubMedCentralCrossRefPubMed
6.
go back to reference Mu J, Myers RA, Jiang H, Liu S, Ricklefs S, Waisberg M, Chotivanich K, Wilairatana P, Krudsood S, White NJ, Udomsangpetch R, Cui L, Ho M, Ou F, Li H, Song J, Li G, Wang X, Seila S, Sokunthea S, Socheat D, Sturdevant DE, Porcella SF, Fairhurst RM, Wellems TE, Awadalla P, Su XZ: Plasmodium falciparum genome-wide scans for positive selection, recombination hot spots and resistance to antimalarial drugs. Nat Genet. 2010, 42: 268-271. 10.1038/ng.528.PubMedCentralCrossRefPubMed Mu J, Myers RA, Jiang H, Liu S, Ricklefs S, Waisberg M, Chotivanich K, Wilairatana P, Krudsood S, White NJ, Udomsangpetch R, Cui L, Ho M, Ou F, Li H, Song J, Li G, Wang X, Seila S, Sokunthea S, Socheat D, Sturdevant DE, Porcella SF, Fairhurst RM, Wellems TE, Awadalla P, Su XZ: Plasmodium falciparum genome-wide scans for positive selection, recombination hot spots and resistance to antimalarial drugs. Nat Genet. 2010, 42: 268-271. 10.1038/ng.528.PubMedCentralCrossRefPubMed
7.
go back to reference Anthony TG, Conway DJ, Cox-Singh J, Matusop A, Ratnam S, Shamsul S, Singh B: Fragmented population structure of Plasmodium falciparum in a region of declining endemicity. J Infect Dis. 2005, 191: 1558-1564. 10.1086/429338.CrossRefPubMed Anthony TG, Conway DJ, Cox-Singh J, Matusop A, Ratnam S, Shamsul S, Singh B: Fragmented population structure of Plasmodium falciparum in a region of declining endemicity. J Infect Dis. 2005, 191: 1558-1564. 10.1086/429338.CrossRefPubMed
8.
go back to reference Iwagami M, Rivera PT, Villacorte EA, Escueta AD, Hatabu T, Kawazu S, Hayakawa T, Tanabe K, Kano S: Genetic diversity and population structure of Plasmodium falciparum in the Philippines. Malar J. 2009, 8: 96-10.1186/1475-2875-8-96.PubMedCentralCrossRefPubMed Iwagami M, Rivera PT, Villacorte EA, Escueta AD, Hatabu T, Kawazu S, Hayakawa T, Tanabe K, Kano S: Genetic diversity and population structure of Plasmodium falciparum in the Philippines. Malar J. 2009, 8: 96-10.1186/1475-2875-8-96.PubMedCentralCrossRefPubMed
9.
go back to reference Bogreau H, Renaud F, Bouchiba H, Durand P, Assi SB, Henry MC, Garnotel E, Pradines B, Fusai T, Wade B, Adehossi E, Parola P, Kamil MA, Puijalon O, Rogier C: Genetic diversity and structure of African Plasmodium falciparum populations in urban and rural areas. Am J Trop Med Hyg. 2006, 74: 953-959.PubMed Bogreau H, Renaud F, Bouchiba H, Durand P, Assi SB, Henry MC, Garnotel E, Pradines B, Fusai T, Wade B, Adehossi E, Parola P, Kamil MA, Puijalon O, Rogier C: Genetic diversity and structure of African Plasmodium falciparum populations in urban and rural areas. Am J Trop Med Hyg. 2006, 74: 953-959.PubMed
10.
go back to reference Durand P, Michalakis Y, Cestier S, Oury B, Leclerc MC, Tibayrenc M, Renaud F: Significant linkage disequilibrium and high genetic diversity in a population of Plasmodium falciparum from an area (Republic of the Congo) highly endemic for malaria. Am J Trop Med Hyg. 2003, 68: 345-349.PubMed Durand P, Michalakis Y, Cestier S, Oury B, Leclerc MC, Tibayrenc M, Renaud F: Significant linkage disequilibrium and high genetic diversity in a population of Plasmodium falciparum from an area (Republic of the Congo) highly endemic for malaria. Am J Trop Med Hyg. 2003, 68: 345-349.PubMed
11.
go back to reference Leclerc MC, Durand P, de Meeus T, Robert V, Renaud F: Genetic diversity and population structure of Plasmodium falciparum isolates from Dakar, Senegal, investigated from microsatellite and antigen determinant loci. Microbes Infect. 2002, 4: 685-692. 10.1016/S1286-4579(02)01587-3.CrossRefPubMed Leclerc MC, Durand P, de Meeus T, Robert V, Renaud F: Genetic diversity and population structure of Plasmodium falciparum isolates from Dakar, Senegal, investigated from microsatellite and antigen determinant loci. Microbes Infect. 2002, 4: 685-692. 10.1016/S1286-4579(02)01587-3.CrossRefPubMed
12.
go back to reference Joy DA, Feng X, Mu J, Furuya T, Chotivanich K, Krettli AU, Ho M, Wang A, White NJ, Suh E, Beerli P, Su XZ: 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, Beerli P, Su XZ: Early origin and recent expansion of Plasmodium falciparum. Science. 2003, 300: 318-321. 10.1126/science.1081449.CrossRefPubMed
13.
go back to reference Muller I, Bockarie M, Alpers M, Smith T: The epidemiology of malaria in Papua New Guinea. Trends Parasitol. 2003, 19: 253-259. 10.1016/S1471-4922(03)00091-6.CrossRefPubMed Muller I, Bockarie M, Alpers M, Smith T: The epidemiology of malaria in Papua New Guinea. Trends Parasitol. 2003, 19: 253-259. 10.1016/S1471-4922(03)00091-6.CrossRefPubMed
14.
go back to reference Cattani JA, Tulloch JL, Vrbova H, Jolley D, Gibson FD, Moir JS, Heywood PF, Alpers MP, Stevenson A, Clancy R: The epidemiology of malaria in a population surrounding Madang, Papua New Guinea. Am J Trop Med Hyg. 1986, 35: 3-15.PubMed Cattani JA, Tulloch JL, Vrbova H, Jolley D, Gibson FD, Moir JS, Heywood PF, Alpers MP, Stevenson A, Clancy R: The epidemiology of malaria in a population surrounding Madang, Papua New Guinea. Am J Trop Med Hyg. 1986, 35: 3-15.PubMed
15.
go back to reference Bockarie MJ, Alexander N, Bockarie F, Ibam E, Barnish G, Alpers M: The late biting habit of parous Anopheles mosquitoes and pre-bedtime exposure of humans to infective female mosquitoes. Trans R Soc Trop Med Hyg. 1996, 90: 23-25. 10.1016/S0035-9203(96)90465-4.CrossRefPubMed Bockarie MJ, Alexander N, Bockarie F, Ibam E, Barnish G, Alpers M: The late biting habit of parous Anopheles mosquitoes and pre-bedtime exposure of humans to infective female mosquitoes. Trans R Soc Trop Med Hyg. 1996, 90: 23-25. 10.1016/S0035-9203(96)90465-4.CrossRefPubMed
16.
go back to reference Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF: Human malaria transmission studies in the Anopheles punctulatus complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. Am J Trop Med Hyg. 1988, 39: 135-144.PubMed Burkot TR, Graves PM, Paru R, Wirtz RA, Heywood PF: Human malaria transmission studies in the Anopheles punctulatus complex in Papua New Guinea: sporozoite rates, inoculation rates, and sporozoite densities. Am J Trop Med Hyg. 1988, 39: 135-144.PubMed
17.
go back to reference Hii JL, Smith T, Mai A, Ibam E, Alpers MP: Comparison between anopheline mosquitoes (Diptera: Culicidae) caught using different methods in a malaria endemic area of Papua New Guinea. Bull Entomol Res. 2000, 90: 211-219. 10.1017/S000748530000033X.CrossRefPubMed Hii JL, Smith T, Mai A, Ibam E, Alpers MP: Comparison between anopheline mosquitoes (Diptera: Culicidae) caught using different methods in a malaria endemic area of Papua New Guinea. Bull Entomol Res. 2000, 90: 211-219. 10.1017/S000748530000033X.CrossRefPubMed
18.
go back to reference Hii JL, Smith T, Vounatsou P, Alexander N, Mai A, Ibam E, Alpers MP: Area effects of bednet use in a malaria-endemic area in Papua New Guinea. Trans R Soc Trop Med Hyg. 2001, 95: 7-13. 10.1016/S0035-9203(01)90315-3.CrossRefPubMed Hii JL, Smith T, Vounatsou P, Alexander N, Mai A, Ibam E, Alpers MP: Area effects of bednet use in a malaria-endemic area in Papua New Guinea. Trans R Soc Trop Med Hyg. 2001, 95: 7-13. 10.1016/S0035-9203(01)90315-3.CrossRefPubMed
19.
go back to reference Kasehagen LJ, Mueller I, McNamara DT, Bockarie MJ, Kiniboro B, Rare L, Lorry K, Kastens W, Reeder JC, Kazura JW, Zimmerman PA: Changing patterns of Plasmodium blood-stage infections in the Wosera region of Papua New Guinea monitored by light microscopy and high throughput PCR diagnosis. Am J Trop Med Hyg. 2006, 75: 588-596.PubMedCentralPubMed Kasehagen LJ, Mueller I, McNamara DT, Bockarie MJ, Kiniboro B, Rare L, Lorry K, Kastens W, Reeder JC, Kazura JW, Zimmerman PA: Changing patterns of Plasmodium blood-stage infections in the Wosera region of Papua New Guinea monitored by light microscopy and high throughput PCR diagnosis. Am J Trop Med Hyg. 2006, 75: 588-596.PubMedCentralPubMed
20.
go back to reference Mueller I, Widmer S, Michel D, Maraga S, McNamara DT, Kiniboro B, Sie A, Smith TA, Zimmerman PA: High sensitivity detection of Plasmodium species reveals positive correlations between infections of different species, shifts in age distribution and reduced local variation in Papua New Guinea. Malar J. 2009, 8: 41-55. 10.1186/1475-2875-8-41.PubMedCentralCrossRefPubMed Mueller I, Widmer S, Michel D, Maraga S, McNamara DT, Kiniboro B, Sie A, Smith TA, Zimmerman PA: High sensitivity detection of Plasmodium species reveals positive correlations between infections of different species, shifts in age distribution and reduced local variation in Papua New Guinea. Malar J. 2009, 8: 41-55. 10.1186/1475-2875-8-41.PubMedCentralCrossRefPubMed
21.
go back to reference Paul RE, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, Paru R, Day KP: Mating patterns in malaria parasite populations of Papua New Guinea. Science. 1995, 269: 1709-1711. 10.1126/science.7569897.CrossRefPubMed Paul RE, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, Paru R, Day KP: Mating patterns in malaria parasite populations of Papua New Guinea. Science. 1995, 269: 1709-1711. 10.1126/science.7569897.CrossRefPubMed
22.
go back to reference Sharp PT: Highlands malaria: malaria in Enga Province of Papua New Guinea. P N G Med J. 1982, 25: 253-260.PubMed Sharp PT: Highlands malaria: malaria in Enga Province of Papua New Guinea. P N G Med J. 1982, 25: 253-260.PubMed
23.
go back to reference Genton B, Al-Yaman F, Ginny M, Taraika J, Alpers MP: Relation of anthropometry to malaria morbidity and immunity in Papua New Guinean children. Am J Clin Nutr. 1998, 68: 734-741.PubMed Genton B, Al-Yaman F, Ginny M, Taraika J, Alpers MP: Relation of anthropometry to malaria morbidity and immunity in Papua New Guinean children. Am J Clin Nutr. 1998, 68: 734-741.PubMed
24.
go back to reference Gibson RS, Heywood A, Yaman C, Sohlstrom A, Thompson LU, Heywood P: Growth in children from the Wosera subdistrict, Papua New Guinea, in relation to energy and protein intakes and zinc status. Am J Clin Nutr. 1991, 53: 782-789.PubMed Gibson RS, Heywood A, Yaman C, Sohlstrom A, Thompson LU, Heywood P: Growth in children from the Wosera subdistrict, Papua New Guinea, in relation to energy and protein intakes and zinc status. Am J Clin Nutr. 1991, 53: 782-789.PubMed
25.
go back to reference Shankar AH: Nutritional modulation of malaria morbidity and mortality. J Infect Dis. 2000, 182 (Suppl 1): S37-53. 10.1086/315906.CrossRefPubMed Shankar AH: Nutritional modulation of malaria morbidity and mortality. J Infect Dis. 2000, 182 (Suppl 1): S37-53. 10.1086/315906.CrossRefPubMed
26.
go back to reference Shankar AH, Genton B, Semba RD, Baisor M, Paino J, Tamja S, Adiguma T, Wu L, Rare L, Tielsch JM, Alpers MP, West KP: Effect of vitamin A supplementation on morbidity due to Plasmodium falciparum in young children in Papua New Guinea: a randomised trial. Lancet. 1999, 354: 203-209. 10.1016/S0140-6736(98)08293-2.CrossRefPubMed Shankar AH, Genton B, Semba RD, Baisor M, Paino J, Tamja S, Adiguma T, Wu L, Rare L, Tielsch JM, Alpers MP, West KP: Effect of vitamin A supplementation on morbidity due to Plasmodium falciparum in young children in Papua New Guinea: a randomised trial. Lancet. 1999, 354: 203-209. 10.1016/S0140-6736(98)08293-2.CrossRefPubMed
27.
go back to reference Hii JL, Smith T, Mai A, Mellor S, Lewis D, Alexander N, Alpers MP: Spatial and temporal variation in abundance of Anopheles (Diptera:Culicidae) in a malaria endemic area in Papua New Guinea. J Med Entomol. 1997, 34: 193-205.CrossRefPubMed Hii JL, Smith T, Mai A, Mellor S, Lewis D, Alexander N, Alpers MP: Spatial and temporal variation in abundance of Anopheles (Diptera:Culicidae) in a malaria endemic area in Papua New Guinea. J Med Entomol. 1997, 34: 193-205.CrossRefPubMed
28.
go back to reference Burkot TR, Dye C, Graves PM: An analysis of some factors determining the sporozoite rates, human blood indexes, and biting rates of members of the Anopheles punctulatus complex in Papua New Guinea. Am J Trop Med Hyg. 1989, 40: 229-234.PubMed Burkot TR, Dye C, Graves PM: An analysis of some factors determining the sporozoite rates, human blood indexes, and biting rates of members of the Anopheles punctulatus complex in Papua New Guinea. Am J Trop Med Hyg. 1989, 40: 229-234.PubMed
29.
go back to reference Lewis MPe: Ethnologue: Languages of the World. 2009, Dallas: SIL International, 16 Lewis MPe: Ethnologue: Languages of the World. 2009, Dallas: SIL International, 16
30.
go back to reference Patel SS, King CL, Mgone CS, Kazura JW, Zimmerman PA: Glycophorin C (Gerbich antigen blood group) and band 3 polymorphisms in two malaria holoendemic regions of Papua New Guinea. Am J Hematol. 2004, 75: 1-5. 10.1002/ajh.10448.PubMedCentralCrossRefPubMed Patel SS, King CL, Mgone CS, Kazura JW, Zimmerman PA: Glycophorin C (Gerbich antigen blood group) and band 3 polymorphisms in two malaria holoendemic regions of Papua New Guinea. Am J Hematol. 2004, 75: 1-5. 10.1002/ajh.10448.PubMedCentralCrossRefPubMed
31.
go back to reference Cooper RD, Waterson DG, Frances SP, Beebe NW, Pluess B, Sweeney AW: Malaria vectors of Papua New Guinea. Int J Parasitol. 2009, 39: 1495-1501. 10.1016/j.ijpara.2009.05.009.CrossRefPubMed Cooper RD, Waterson DG, Frances SP, Beebe NW, Pluess B, Sweeney AW: Malaria vectors of Papua New Guinea. Int J Parasitol. 2009, 39: 1495-1501. 10.1016/j.ijpara.2009.05.009.CrossRefPubMed
32.
go back to reference Cooper RD, Waterson DG, Frances SP, Beebe NW, Sweeney AW: Speciation and distribution of the members of the Anopheles punctulatus (Diptera: Culicidae) group in Papua New Guinea. J Med Entomol. 2002, 39: 16-27. 10.1603/0022-2585-39.1.16.CrossRefPubMed Cooper RD, Waterson DG, Frances SP, Beebe NW, Sweeney AW: Speciation and distribution of the members of the Anopheles punctulatus (Diptera: Culicidae) group in Papua New Guinea. J Med Entomol. 2002, 39: 16-27. 10.1603/0022-2585-39.1.16.CrossRefPubMed
33.
go back to reference Benet A, Mai A, Bockarie F, Lagog M, Zimmerman P, Alpers MP, Reeder JC, Bockarie MJ: Polymerase chain reaction diagnosis and the changing pattern of vector ecology and malaria transmission dynamics in papua new Guinea. Am J Trop Med Hyg. 2004, 71: 277-284.PubMed Benet A, Mai A, Bockarie F, Lagog M, Zimmerman P, Alpers MP, Reeder JC, Bockarie MJ: Polymerase chain reaction diagnosis and the changing pattern of vector ecology and malaria transmission dynamics in papua new Guinea. Am J Trop Med Hyg. 2004, 71: 277-284.PubMed
34.
go back to reference Forsyth KP, Anders RF, Cattani JA, Alpers MP: Small area variation in prevalence of an S-antigen serotype of Plasmodium falciparum in villages of Madang, Papua New Guinea. Am J Trop Med Hyg. 1989, 40: 344-350.PubMed Forsyth KP, Anders RF, Cattani JA, Alpers MP: Small area variation in prevalence of an S-antigen serotype of Plasmodium falciparum in villages of Madang, Papua New Guinea. Am J Trop Med Hyg. 1989, 40: 344-350.PubMed
35.
go back to reference Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP: Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999, 119: 113-125. 10.1017/S0031182099004552.CrossRefPubMed Anderson TJ, Su XZ, Bockarie M, Lagog M, Day KP: Twelve microsatellite markers for characterization of Plasmodium falciparum from finger-prick blood samples. Parasitology. 1999, 119: 113-125. 10.1017/S0031182099004552.CrossRefPubMed
36.
go back to reference Falk N, Maire N, Sama W, Owusu-Agyei S, Smith T, Beck HP, Felger I: Comparison of PCR-RFLP and Genescan-based genotyping for analyzing infection dynamics of Plasmodium falciparum. Am J Trop Med Hyg. 2006, 74: 944-950.PubMed Falk N, Maire N, Sama W, Owusu-Agyei S, Smith T, Beck HP, Felger I: Comparison of PCR-RFLP and Genescan-based genotyping for analyzing infection dynamics of Plasmodium falciparum. Am J Trop Med Hyg. 2006, 74: 944-950.PubMed
37.
go back to reference Glaubitz JC: CONVERT: A user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Molecular Ecology Notes. 2004, 4: 309-310. 10.1111/j.1471-8286.2004.00597.x.CrossRef Glaubitz JC: CONVERT: A user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Molecular Ecology Notes. 2004, 4: 309-310. 10.1111/j.1471-8286.2004.00597.x.CrossRef
38.
go back to reference Excoffier L, Laval 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, Laval G, Schneider S: Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online. 2005, 1: 47-50.PubMedCentral
39.
go back to reference Hurlbert SH: The non-concept of species diversity: a critique and alternative parameters. Ecology. 1971, 52: 577-586. 10.2307/1934145.CrossRef Hurlbert SH: The non-concept of species diversity: a critique and alternative parameters. Ecology. 1971, 52: 577-586. 10.2307/1934145.CrossRef
40.
go back to reference Goudet J: FSTAT (Version 1.2): A computer program to calculate F-statistics. Journal of Heredity. 1995, 86: 485-486. Goudet J: FSTAT (Version 1.2): A computer program to calculate F-statistics. Journal of Heredity. 1995, 86: 485-486.
41.
go back to reference Haubold B, Hudson RR: LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage Analysis. Bioinformatics. 2000, 16: 847-848. 10.1093/bioinformatics/16.9.847.CrossRefPubMed Haubold B, Hudson RR: LIAN 3.0: detecting linkage disequilibrium in multilocus data. Linkage Analysis. Bioinformatics. 2000, 16: 847-848. 10.1093/bioinformatics/16.9.847.CrossRefPubMed
42.
go back to reference Michalakis Y, Excoffier L: A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics. 1996, 142: 1061-1064.PubMedCentralPubMed Michalakis Y, Excoffier L: A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics. 1996, 142: 1061-1064.PubMedCentralPubMed
43.
go back to reference Slatkin M: A measure of population subdivision based on microsatellite allele frequencies. Genetics. 1995, 139: 457-462.PubMedCentralPubMed Slatkin M: A measure of population subdivision based on microsatellite allele frequencies. Genetics. 1995, 139: 457-462.PubMedCentralPubMed
44.
go back to reference Anderson TJ, Su XZ, Roddam A, Day KP: Complex mutations in a high proportion of microsatellite loci from the protozoan parasite Plasmodium falciparum. Mol Ecol. 2000, 9: 1599-1608. 10.1046/j.1365-294x.2000.01057.x.CrossRefPubMed Anderson TJ, Su XZ, Roddam A, Day KP: Complex mutations in a high proportion of microsatellite loci from the protozoan parasite Plasmodium falciparum. Mol Ecol. 2000, 9: 1599-1608. 10.1046/j.1365-294x.2000.01057.x.CrossRefPubMed
45.
go back to reference Manly BJF: Randomisation and Monte Carlo methods in biology. 1991, London: Chapman and HallCrossRef Manly BJF: Randomisation and Monte Carlo methods in biology. 1991, London: Chapman and HallCrossRef
46.
go back to reference Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. 2000, 155: 945- Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. 2000, 155: 945-
48.
go back to reference Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005, 14: 2611-2620. 10.1111/j.1365-294X.2005.02553.x.CrossRefPubMed Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005, 14: 2611-2620. 10.1111/j.1365-294X.2005.02553.x.CrossRefPubMed
49.
go back to reference Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T: Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13: 2498-2504. 10.1101/gr.1239303.PubMedCentralCrossRefPubMed Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T: Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003, 13: 2498-2504. 10.1101/gr.1239303.PubMedCentralCrossRefPubMed
50.
go back to reference Kamada TaK S: A simple method for computing general position in displaying three-dimensional objects. Computer Vision, Graphics and Image Processing. 1988, 41: 43-56. 10.1016/0734-189X(88)90116-8.CrossRef Kamada TaK S: A simple method for computing general position in displaying three-dimensional objects. Computer Vision, Graphics and Image Processing. 1988, 41: 43-56. 10.1016/0734-189X(88)90116-8.CrossRef
52.
go back to reference Li CC: Population Genetics. 1955, Chicago: University of Chicago Press Li CC: Population Genetics. 1955, Chicago: University of Chicago Press
53.
go back to reference Annan Z, Durand P, Ayala FJ, Arnathau C, Awono-Ambene P, Simard F, Razakandrainibe FG, Koella JC, Fontenille D, Renaud F: Population genetic structure of Plasmodium falciparum in the two main African vectors, Anopheles gambiae and Anopheles funestus. Proc Natl Acad Sci USA. 2007, 104: 7987-7992. 10.1073/pnas.0702715104.PubMedCentralCrossRefPubMed Annan Z, Durand P, Ayala FJ, Arnathau C, Awono-Ambene P, Simard F, Razakandrainibe FG, Koella JC, Fontenille D, Renaud F: Population genetic structure of Plasmodium falciparum in the two main African vectors, Anopheles gambiae and Anopheles funestus. Proc Natl Acad Sci USA. 2007, 104: 7987-7992. 10.1073/pnas.0702715104.PubMedCentralCrossRefPubMed
Metadata
Title
Multilocus haplotypes reveal variable levels of diversity and population structure of Plasmodium falciparum in Papua New Guinea, a region of intense perennial transmission
Authors
Lee Schultz
Johanna Wapling
Ivo Mueller
Pilate O Ntsuke
Nicolas Senn
Joe Nale
Benson Kiniboro
Caroline O Buckee
Livingstone Tavul
Peter M Siba
John C Reeder
Alyssa E Barry
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2010
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-9-336

Other articles of this Issue 1/2010

Malaria Journal 1/2010 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.