Origin and diversification of the human parasite Schistosoma mansoni

Jess A T Morgan, Randall J. Dejong, Grace O. Adeoye, Ebenezer D O Ansa, ConstanÇa S. Barbosa, Philippe Brémond, Italo M. Cesari, Nathalie Charbonnel, Lygia R. Corrêa, Godefroy Coulibaly, Paulo Sérgio D'Andrea, Cecilia Pereira De Souza, Michael J. Doenhoff, Sharon File, Mohamed A. Idris, R. Nino Incani, Philippe Jarne, Diana M S Karanja, Francis Kazibwe, John Kpikpi & 16 others Nicholas J S Lwambo, Amadou Mabaye, Luiz A. Magalhães, Asanteli Makundi, Hélène Moné, Gabriel Mouahid, Gerald M. Muchemi, Ben N. Mungai, Mariama Séne, Vaughan Southgate, Louis Albert Tchuem Tchuenté, Andre Théron, Fouad Yousif, Eliana M. Zanotti-Magalhães, Gerald M. Mkoji, Eric S. Loker

Research output: Contribution to journalArticle

79 Citations (Scopus)

Abstract

Schistosoma mansoni is the most widespread of the human-infecting schistosomes, present in 54 countries, predominantly in Africa, but also in Madagascar, the Arabian Peninsula, and the Neotropics. Adult-stage parasites that infect humans are also occasionally recovered from baboons, rodents, and other mammals. Larval stages of the parasite are dependent upon certain species of freshwater snails in the genus Biomphalaria, which largely determine the parasite's geographical range. How S. mansoni genetic diversity is distributed geographically and among isolates using different hosts has never been examined with DNA sequence data. Here we describe the global phylogeography of S. mansoni using more than 2500 bp of mitochondrial DNA (mtDNA) from 143 parasites collected in 53 geographically widespread localities. Considerable within-species mtDNA diversity was found, with 85 unique haplotypes grouping into five distinct lineages. Geographical separation, and not host use, appears to be the most important factor in the diversification of the parasite. East African specimens showed a remarkable amount of variation, comprising three clades and basal members of a fourth, strongly suggesting an East African origin for the parasite 0.30-0.43 million years ago, a time frame that follows the arrival of its snail host. Less but still substantial variation was found in the rest of Africa. A recent colonization of the New World is supported by finding only seven closely related New World haplotypes which have West African affinities. All Brazilian isolates have nearly identical mtDNA haplotypes, suggesting a founder effect from the establishment and spread of the parasite in this large country.

Original languageEnglish
Pages (from-to)3889-3902
Number of pages14
JournalMolecular Ecology
Volume14
Issue number12
DOIs
Publication statusPublished - Oct 2005

Fingerprint

Schistosoma mansoni
parasite
Parasites
parasites
Mitochondrial DNA
mitochondrial DNA
Haplotypes
haplotypes
Snails
snail
snails
Biomphalaria
Phylogeography
Founder Effect
host use
Madagascar
founder effect
Mammals
Schistosoma
Papio

Keywords

  • Africa
  • Biomphalaria
  • Brazil
  • Phylogeography
  • Schistosomiasis
  • Slave trade

ASJC Scopus subject areas

  • Ecology
  • Biochemistry, Genetics and Molecular Biology(all)
  • Biochemistry

Cite this

Morgan, J. A. T., Dejong, R. J., Adeoye, G. O., Ansa, E. D. O., Barbosa, C. S., Brémond, P., ... Loker, E. S. (2005). Origin and diversification of the human parasite Schistosoma mansoni. Molecular Ecology, 14(12), 3889-3902. https://doi.org/10.1111/j.1365-294X.2005.02709.x

Origin and diversification of the human parasite Schistosoma mansoni. / Morgan, Jess A T; Dejong, Randall J.; Adeoye, Grace O.; Ansa, Ebenezer D O; Barbosa, ConstanÇa S.; Brémond, Philippe; Cesari, Italo M.; Charbonnel, Nathalie; Corrêa, Lygia R.; Coulibaly, Godefroy; D'Andrea, Paulo Sérgio; De Souza, Cecilia Pereira; Doenhoff, Michael J.; File, Sharon; Idris, Mohamed A.; Incani, R. Nino; Jarne, Philippe; Karanja, Diana M S; Kazibwe, Francis; Kpikpi, John; Lwambo, Nicholas J S; Mabaye, Amadou; Magalhães, Luiz A.; Makundi, Asanteli; Moné, Hélène; Mouahid, Gabriel; Muchemi, Gerald M.; Mungai, Ben N.; Séne, Mariama; Southgate, Vaughan; Tchuenté, Louis Albert Tchuem; Théron, Andre; Yousif, Fouad; Zanotti-Magalhães, Eliana M.; Mkoji, Gerald M.; Loker, Eric S.

In: Molecular Ecology, Vol. 14, No. 12, 10.2005, p. 3889-3902.

Research output: Contribution to journalArticle

Morgan, JAT, Dejong, RJ, Adeoye, GO, Ansa, EDO, Barbosa, CS, Brémond, P, Cesari, IM, Charbonnel, N, Corrêa, LR, Coulibaly, G, D'Andrea, PS, De Souza, CP, Doenhoff, MJ, File, S, Idris, MA, Incani, RN, Jarne, P, Karanja, DMS, Kazibwe, F, Kpikpi, J, Lwambo, NJS, Mabaye, A, Magalhães, LA, Makundi, A, Moné, H, Mouahid, G, Muchemi, GM, Mungai, BN, Séne, M, Southgate, V, Tchuenté, LAT, Théron, A, Yousif, F, Zanotti-Magalhães, EM, Mkoji, GM & Loker, ES 2005, 'Origin and diversification of the human parasite Schistosoma mansoni', Molecular Ecology, vol. 14, no. 12, pp. 3889-3902. https://doi.org/10.1111/j.1365-294X.2005.02709.x
Morgan JAT, Dejong RJ, Adeoye GO, Ansa EDO, Barbosa CS, Brémond P et al. Origin and diversification of the human parasite Schistosoma mansoni. Molecular Ecology. 2005 Oct;14(12):3889-3902. https://doi.org/10.1111/j.1365-294X.2005.02709.x
Morgan, Jess A T ; Dejong, Randall J. ; Adeoye, Grace O. ; Ansa, Ebenezer D O ; Barbosa, ConstanÇa S. ; Brémond, Philippe ; Cesari, Italo M. ; Charbonnel, Nathalie ; Corrêa, Lygia R. ; Coulibaly, Godefroy ; D'Andrea, Paulo Sérgio ; De Souza, Cecilia Pereira ; Doenhoff, Michael J. ; File, Sharon ; Idris, Mohamed A. ; Incani, R. Nino ; Jarne, Philippe ; Karanja, Diana M S ; Kazibwe, Francis ; Kpikpi, John ; Lwambo, Nicholas J S ; Mabaye, Amadou ; Magalhães, Luiz A. ; Makundi, Asanteli ; Moné, Hélène ; Mouahid, Gabriel ; Muchemi, Gerald M. ; Mungai, Ben N. ; Séne, Mariama ; Southgate, Vaughan ; Tchuenté, Louis Albert Tchuem ; Théron, Andre ; Yousif, Fouad ; Zanotti-Magalhães, Eliana M. ; Mkoji, Gerald M. ; Loker, Eric S. / Origin and diversification of the human parasite Schistosoma mansoni. In: Molecular Ecology. 2005 ; Vol. 14, No. 12. pp. 3889-3902.
@article{9d2d2708895d4b5fa52ac8bc464d4bc6,
title = "Origin and diversification of the human parasite Schistosoma mansoni",
abstract = "Schistosoma mansoni is the most widespread of the human-infecting schistosomes, present in 54 countries, predominantly in Africa, but also in Madagascar, the Arabian Peninsula, and the Neotropics. Adult-stage parasites that infect humans are also occasionally recovered from baboons, rodents, and other mammals. Larval stages of the parasite are dependent upon certain species of freshwater snails in the genus Biomphalaria, which largely determine the parasite's geographical range. How S. mansoni genetic diversity is distributed geographically and among isolates using different hosts has never been examined with DNA sequence data. Here we describe the global phylogeography of S. mansoni using more than 2500 bp of mitochondrial DNA (mtDNA) from 143 parasites collected in 53 geographically widespread localities. Considerable within-species mtDNA diversity was found, with 85 unique haplotypes grouping into five distinct lineages. Geographical separation, and not host use, appears to be the most important factor in the diversification of the parasite. East African specimens showed a remarkable amount of variation, comprising three clades and basal members of a fourth, strongly suggesting an East African origin for the parasite 0.30-0.43 million years ago, a time frame that follows the arrival of its snail host. Less but still substantial variation was found in the rest of Africa. A recent colonization of the New World is supported by finding only seven closely related New World haplotypes which have West African affinities. All Brazilian isolates have nearly identical mtDNA haplotypes, suggesting a founder effect from the establishment and spread of the parasite in this large country.",
keywords = "Africa, Biomphalaria, Brazil, Phylogeography, Schistosomiasis, Slave trade",
author = "Morgan, {Jess A T} and Dejong, {Randall J.} and Adeoye, {Grace O.} and Ansa, {Ebenezer D O} and Barbosa, {Constan{\cC}a S.} and Philippe Br{\'e}mond and Cesari, {Italo M.} and Nathalie Charbonnel and Corr{\^e}a, {Lygia R.} and Godefroy Coulibaly and D'Andrea, {Paulo S{\'e}rgio} and {De Souza}, {Cecilia Pereira} and Doenhoff, {Michael J.} and Sharon File and Idris, {Mohamed A.} and Incani, {R. Nino} and Philippe Jarne and Karanja, {Diana M S} and Francis Kazibwe and John Kpikpi and Lwambo, {Nicholas J S} and Amadou Mabaye and Magalh{\~a}es, {Luiz A.} and Asanteli Makundi and H{\'e}l{\`e}ne Mon{\'e} and Gabriel Mouahid and Muchemi, {Gerald M.} and Mungai, {Ben N.} and Mariama S{\'e}ne and Vaughan Southgate and Tchuent{\'e}, {Louis Albert Tchuem} and Andre Th{\'e}ron and Fouad Yousif and Zanotti-Magalh{\~a}es, {Eliana M.} and Mkoji, {Gerald M.} and Loker, {Eric S.}",
year = "2005",
month = "10",
doi = "10.1111/j.1365-294X.2005.02709.x",
language = "English",
volume = "14",
pages = "3889--3902",
journal = "Molecular Ecology",
issn = "0962-1083",
publisher = "Wiley-Blackwell",
number = "12",

}

TY - JOUR

T1 - Origin and diversification of the human parasite Schistosoma mansoni

AU - Morgan, Jess A T

AU - Dejong, Randall J.

AU - Adeoye, Grace O.

AU - Ansa, Ebenezer D O

AU - Barbosa, ConstanÇa S.

AU - Brémond, Philippe

AU - Cesari, Italo M.

AU - Charbonnel, Nathalie

AU - Corrêa, Lygia R.

AU - Coulibaly, Godefroy

AU - D'Andrea, Paulo Sérgio

AU - De Souza, Cecilia Pereira

AU - Doenhoff, Michael J.

AU - File, Sharon

AU - Idris, Mohamed A.

AU - Incani, R. Nino

AU - Jarne, Philippe

AU - Karanja, Diana M S

AU - Kazibwe, Francis

AU - Kpikpi, John

AU - Lwambo, Nicholas J S

AU - Mabaye, Amadou

AU - Magalhães, Luiz A.

AU - Makundi, Asanteli

AU - Moné, Hélène

AU - Mouahid, Gabriel

AU - Muchemi, Gerald M.

AU - Mungai, Ben N.

AU - Séne, Mariama

AU - Southgate, Vaughan

AU - Tchuenté, Louis Albert Tchuem

AU - Théron, Andre

AU - Yousif, Fouad

AU - Zanotti-Magalhães, Eliana M.

AU - Mkoji, Gerald M.

AU - Loker, Eric S.

PY - 2005/10

Y1 - 2005/10

N2 - Schistosoma mansoni is the most widespread of the human-infecting schistosomes, present in 54 countries, predominantly in Africa, but also in Madagascar, the Arabian Peninsula, and the Neotropics. Adult-stage parasites that infect humans are also occasionally recovered from baboons, rodents, and other mammals. Larval stages of the parasite are dependent upon certain species of freshwater snails in the genus Biomphalaria, which largely determine the parasite's geographical range. How S. mansoni genetic diversity is distributed geographically and among isolates using different hosts has never been examined with DNA sequence data. Here we describe the global phylogeography of S. mansoni using more than 2500 bp of mitochondrial DNA (mtDNA) from 143 parasites collected in 53 geographically widespread localities. Considerable within-species mtDNA diversity was found, with 85 unique haplotypes grouping into five distinct lineages. Geographical separation, and not host use, appears to be the most important factor in the diversification of the parasite. East African specimens showed a remarkable amount of variation, comprising three clades and basal members of a fourth, strongly suggesting an East African origin for the parasite 0.30-0.43 million years ago, a time frame that follows the arrival of its snail host. Less but still substantial variation was found in the rest of Africa. A recent colonization of the New World is supported by finding only seven closely related New World haplotypes which have West African affinities. All Brazilian isolates have nearly identical mtDNA haplotypes, suggesting a founder effect from the establishment and spread of the parasite in this large country.

AB - Schistosoma mansoni is the most widespread of the human-infecting schistosomes, present in 54 countries, predominantly in Africa, but also in Madagascar, the Arabian Peninsula, and the Neotropics. Adult-stage parasites that infect humans are also occasionally recovered from baboons, rodents, and other mammals. Larval stages of the parasite are dependent upon certain species of freshwater snails in the genus Biomphalaria, which largely determine the parasite's geographical range. How S. mansoni genetic diversity is distributed geographically and among isolates using different hosts has never been examined with DNA sequence data. Here we describe the global phylogeography of S. mansoni using more than 2500 bp of mitochondrial DNA (mtDNA) from 143 parasites collected in 53 geographically widespread localities. Considerable within-species mtDNA diversity was found, with 85 unique haplotypes grouping into five distinct lineages. Geographical separation, and not host use, appears to be the most important factor in the diversification of the parasite. East African specimens showed a remarkable amount of variation, comprising three clades and basal members of a fourth, strongly suggesting an East African origin for the parasite 0.30-0.43 million years ago, a time frame that follows the arrival of its snail host. Less but still substantial variation was found in the rest of Africa. A recent colonization of the New World is supported by finding only seven closely related New World haplotypes which have West African affinities. All Brazilian isolates have nearly identical mtDNA haplotypes, suggesting a founder effect from the establishment and spread of the parasite in this large country.

KW - Africa

KW - Biomphalaria

KW - Brazil

KW - Phylogeography

KW - Schistosomiasis

KW - Slave trade

UR - http://www.scopus.com/inward/record.url?scp=33644669157&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33644669157&partnerID=8YFLogxK

U2 - 10.1111/j.1365-294X.2005.02709.x

DO - 10.1111/j.1365-294X.2005.02709.x

M3 - Article

VL - 14

SP - 3889

EP - 3902

JO - Molecular Ecology

JF - Molecular Ecology

SN - 0962-1083

IS - 12

ER -