Whole-Genome Scans Provide Evidence of Adaptive Evolution in Malawian Plasmodium falciparum Isolates

Harold Ocholla; Mark D Preston; Mwapatsa Mipando; Anja Tatiana Ramstedt Jensen; Susana Campino; Bronwyn MacInnis; Daniel Alcock; Anja Terlouw; Issaka Zongo; Jean-Bosco Oudraogo; Abdoulaye A Djimde; Samuel Assefa; Ogobara K Doumbo; Steffen Borrmann; Alexis Nzila; Kevin Marsh; Rick M Fairhurst; Francois Nosten; Tim J C Anderson; Dominic P Kwiatkowski; Alister Craig; Taane G Clark; Jacqui Montgomery

doi:10.1093/infdis/jiu349

Whole-Genome Scans Provide Evidence of Adaptive Evolution in Malawian Plasmodium falciparum Isolates

Harold Ocholla, Mark D Preston, Mwapatsa Mipando, Anja Tatiana Ramstedt Jensen, Susana Campino, Bronwyn MacInnis, Daniel Alcock, Anja Terlouw, Issaka Zongo, Jean-Bosco Oudraogo, Abdoulaye A Djimde, Samuel Assefa, Ogobara K Doumbo, Steffen Borrmann, Alexis Nzila, Kevin Marsh, Rick M Fairhurst, Francois Nosten, Tim J C Anderson, Dominic P KwiatkowskiAlister Craig, Taane G Clark, Jacqui Montgomery

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Abstract

BACKGROUND: Selection by host immunity and antimalarial drugs has driven extensive adaptive evolution in Plasmodium falciparum and continues to produce ever-changing landscapes of genetic variation.

METHODS: We performed whole-genome sequencing of 69 P. falciparum isolates from Malawi and used population genetics approaches to investigate genetic diversity and population structure and identify loci under selection.

RESULTS: High genetic diversity (π = 2.4 × 10(-4)), moderately high multiplicity of infection (2.7), and low linkage disequilibrium (500-bp) were observed in Chikhwawa District, Malawi, an area of high malaria transmission. Allele frequency-based tests provided evidence of recent population growth in Malawi and detected potential targets of host immunity and candidate vaccine antigens. Comparison of the sequence variation between isolates from Malawi and those from 5 geographically dispersed countries (Kenya, Burkina Faso, Mali, Cambodia, and Thailand) detected population genetic differences between Africa and Asia, within Southeast Asia, and within Africa. Haplotype-based tests of selection to sequence data from all 6 populations identified signals of directional selection at known drug-resistance loci, including pfcrt, pfdhps, pfmdr1, and pfgch1.

CONCLUSIONS: The sequence variations observed at drug-resistance loci reflect differences in each country's historical use of antimalarial drugs and may be useful in formulating local malaria treatment guidelines.

Originalsprog	Engelsk
Tidsskrift	The Journal of Infectious Diseases
Vol/bind	210
Udgave nummer	12
Sider (fra-til)	1991-2000
Antal sider	10
ISSN	0022-1899
DOI	https://doi.org/10.1093/infdis/jiu349
Status	Udgivet - dec. 2014

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10.1093/infdis/jiu349

Whole-genome scans provide evidence of adaptive evolution in Malawian Plasmodium falciparum isolates.Forlagets udgivne version, 323 KB

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Ocholla, H., Preston, M. D., Mipando, M., Jensen, A. T. R., Campino, S., MacInnis, B., Alcock, D., Terlouw, A., Zongo, I., Oudraogo, J-B., Djimde, A. A., Assefa, S., Doumbo, O. K., Borrmann, S., Nzila, A., Marsh, K., Fairhurst, R. M., Nosten, F., Anderson, T. J. C., ... Montgomery, J. (2014). Whole-Genome Scans Provide Evidence of Adaptive Evolution in Malawian Plasmodium falciparum Isolates. The Journal of Infectious Diseases, 210(12), 1991-2000. https://doi.org/10.1093/infdis/jiu349

Ocholla, H, Preston, MD, Mipando, M, Jensen, ATR, Campino, S, MacInnis, B, Alcock, D, Terlouw, A, Zongo, I, Oudraogo, J-B, Djimde, AA, Assefa, S, Doumbo, OK, Borrmann, S, Nzila, A, Marsh, K, Fairhurst, RM, Nosten, F, Anderson, TJC, Kwiatkowski, DP, Craig, A, Clark, TG & Montgomery, J 2014, 'Whole-Genome Scans Provide Evidence of Adaptive Evolution in Malawian Plasmodium falciparum Isolates', The Journal of Infectious Diseases, bind 210, nr. 12, s. 1991-2000. https://doi.org/10.1093/infdis/jiu349

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title = "Whole-Genome Scans Provide Evidence of Adaptive Evolution in Malawian Plasmodium falciparum Isolates",

abstract = "BACKGROUND: Selection by host immunity and antimalarial drugs has driven extensive adaptive evolution in Plasmodium falciparum and continues to produce ever-changing landscapes of genetic variation.METHODS: We performed whole-genome sequencing of 69 P. falciparum isolates from Malawi and used population genetics approaches to investigate genetic diversity and population structure and identify loci under selection.RESULTS: High genetic diversity (π = 2.4 × 10(-4)), moderately high multiplicity of infection (2.7), and low linkage disequilibrium (500-bp) were observed in Chikhwawa District, Malawi, an area of high malaria transmission. Allele frequency-based tests provided evidence of recent population growth in Malawi and detected potential targets of host immunity and candidate vaccine antigens. Comparison of the sequence variation between isolates from Malawi and those from 5 geographically dispersed countries (Kenya, Burkina Faso, Mali, Cambodia, and Thailand) detected population genetic differences between Africa and Asia, within Southeast Asia, and within Africa. Haplotype-based tests of selection to sequence data from all 6 populations identified signals of directional selection at known drug-resistance loci, including pfcrt, pfdhps, pfmdr1, and pfgch1.CONCLUSIONS: The sequence variations observed at drug-resistance loci reflect differences in each country's historical use of antimalarial drugs and may be useful in formulating local malaria treatment guidelines.",

author = "Harold Ocholla and Preston, {Mark D} and Mwapatsa Mipando and Jensen, {Anja Tatiana Ramstedt} and Susana Campino and Bronwyn MacInnis and Daniel Alcock and Anja Terlouw and Issaka Zongo and Jean-Bosco Oudraogo and Djimde, {Abdoulaye A} and Samuel Assefa and Doumbo, {Ogobara K} and Steffen Borrmann and Alexis Nzila and Kevin Marsh and Fairhurst, {Rick M} and Francois Nosten and Anderson, {Tim J C} and Kwiatkowski, {Dominic P} and Alister Craig and Clark, {Taane G} and Jacqui Montgomery",

note = "{\textcopyright} The Author 2014. Published by Oxford University Press on behalf of the Infectious Diseases Society of America.",

year = "2014",

month = dec,

doi = "10.1093/infdis/jiu349",

language = "English",

volume = "210",

pages = "1991--2000",

journal = "Journal of Infectious Diseases",

issn = "0022-1899",

publisher = "Oxford University Press",

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T1 - Whole-Genome Scans Provide Evidence of Adaptive Evolution in Malawian Plasmodium falciparum Isolates

AU - Ocholla, Harold

AU - Preston, Mark D

AU - Mipando, Mwapatsa

AU - Jensen, Anja Tatiana Ramstedt

AU - Campino, Susana

AU - MacInnis, Bronwyn

AU - Alcock, Daniel

AU - Terlouw, Anja

AU - Zongo, Issaka

AU - Oudraogo, Jean-Bosco

AU - Djimde, Abdoulaye A

AU - Assefa, Samuel

AU - Doumbo, Ogobara K

AU - Borrmann, Steffen

AU - Nzila, Alexis

AU - Marsh, Kevin

AU - Fairhurst, Rick M

AU - Nosten, Francois

AU - Anderson, Tim J C

AU - Kwiatkowski, Dominic P

AU - Craig, Alister

AU - Clark, Taane G

AU - Montgomery, Jacqui

PY - 2014/12

Y1 - 2014/12

N2 - BACKGROUND: Selection by host immunity and antimalarial drugs has driven extensive adaptive evolution in Plasmodium falciparum and continues to produce ever-changing landscapes of genetic variation.METHODS: We performed whole-genome sequencing of 69 P. falciparum isolates from Malawi and used population genetics approaches to investigate genetic diversity and population structure and identify loci under selection.RESULTS: High genetic diversity (π = 2.4 × 10(-4)), moderately high multiplicity of infection (2.7), and low linkage disequilibrium (500-bp) were observed in Chikhwawa District, Malawi, an area of high malaria transmission. Allele frequency-based tests provided evidence of recent population growth in Malawi and detected potential targets of host immunity and candidate vaccine antigens. Comparison of the sequence variation between isolates from Malawi and those from 5 geographically dispersed countries (Kenya, Burkina Faso, Mali, Cambodia, and Thailand) detected population genetic differences between Africa and Asia, within Southeast Asia, and within Africa. Haplotype-based tests of selection to sequence data from all 6 populations identified signals of directional selection at known drug-resistance loci, including pfcrt, pfdhps, pfmdr1, and pfgch1.CONCLUSIONS: The sequence variations observed at drug-resistance loci reflect differences in each country's historical use of antimalarial drugs and may be useful in formulating local malaria treatment guidelines.

AB - BACKGROUND: Selection by host immunity and antimalarial drugs has driven extensive adaptive evolution in Plasmodium falciparum and continues to produce ever-changing landscapes of genetic variation.METHODS: We performed whole-genome sequencing of 69 P. falciparum isolates from Malawi and used population genetics approaches to investigate genetic diversity and population structure and identify loci under selection.RESULTS: High genetic diversity (π = 2.4 × 10(-4)), moderately high multiplicity of infection (2.7), and low linkage disequilibrium (500-bp) were observed in Chikhwawa District, Malawi, an area of high malaria transmission. Allele frequency-based tests provided evidence of recent population growth in Malawi and detected potential targets of host immunity and candidate vaccine antigens. Comparison of the sequence variation between isolates from Malawi and those from 5 geographically dispersed countries (Kenya, Burkina Faso, Mali, Cambodia, and Thailand) detected population genetic differences between Africa and Asia, within Southeast Asia, and within Africa. Haplotype-based tests of selection to sequence data from all 6 populations identified signals of directional selection at known drug-resistance loci, including pfcrt, pfdhps, pfmdr1, and pfgch1.CONCLUSIONS: The sequence variations observed at drug-resistance loci reflect differences in each country's historical use of antimalarial drugs and may be useful in formulating local malaria treatment guidelines.

U2 - 10.1093/infdis/jiu349

DO - 10.1093/infdis/jiu349

M3 - Journal article

C2 - 24948693

SN - 0022-1899

VL - 210

SP - 1991

EP - 2000

JO - Journal of Infectious Diseases

JF - Journal of Infectious Diseases

IS - 12

ER -

Whole-Genome Scans Provide Evidence of Adaptive Evolution in Malawian Plasmodium falciparum Isolates

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