Trypanosoma vivax displays a clonal population structure

International Journal for Parasitology

Volumn 39, Issue 13, 2009, Pages 1475-1483

  Duffy, Craig W ^a,b   Morrison, Liam J ^a   Black, Alana ^b   Pinchbeck, Gina L ^c   Christley, Robert M ^c   Schoenefeld, Andreas ^d   Tait, Andy ^a   Turner, C Michael R ^b   MacLeod, Annette ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

^d International Trypanotolerance Centre Gambia   (Gambia)

Author keywords

Mating; Microsatellites; Multilocus genotypes; Population genetics; Trypanosoma vivax

Indexed keywords

CLONAL ORGANISM; DISEASE; GENOTYPE; LIVESTOCK; MATING BEHAVIOR; PEST SPECIES; POPULATION GENETICS; POPULATION STRUCTURE;

ARTICLE; CLONAL VARIATION; CONTROLLED STUDY; GENE LINKAGE DISEQUILIBRIUM; GENETIC ANALYSIS; GENOTYPE; HOMOZYGOTE; INHERITANCE; MATING; MEIOSIS; MICROSATELLITE MARKER; NONHUMAN; ORTHOLOGY; POPULATION DYNAMICS; POPULATION GENETICS; PROTOZOAL GENETICS; SYMPATRY; TRYPANOSOMA VIVAX;

ANIMALS; CATTLE; COPULATION; EQUIDAE; GAMBIA; GENOTYPE; GOATS; HORSES; HOST SPECIFICITY; HUMANS; LIVESTOCK; MICROSATELLITE REPEATS; POLYMERASE CHAIN REACTION; TRYPANOSOMA VIVAX;

AFRICA; SUB-SAHARAN AFRICA;

ANIMALIA; BOS; CAPRA HIRCUS; EQUIDAE; GLOSSINA (GENUS); KINETOPLASTIDA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CONGOLENSE; TRYPANOSOMA CRUZI; TRYPANOSOMA VIVAX;

EID: 69349098515     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2009.05.012     Document Type: Article

References (64)

1. Allsopp B.A., and Newton S.D. Characterization of Trypanosoma (Duttonella) vivax by isoenzyme analysis. Int. J. Parasitol. 15 (1985) 265-270
2. Auty H., Mundy A., Fyumagwa R.D., Picozzi K., Welburn S., and Hoare R. Health management of horses under high challenge from trypanosomes: a case study from Serengeti, Tanzania. Vet. Parasitol. 154 (2008) 233-241
3. Batista J.S., Riet-Correa F., Teixeira M.M.G., Madruga C.R., Simões S.D.V., and Maia T.F. Trypanosomiasis by Trypanosoma vivax in cattle in the Brazilian semiarid: description of an outbreak and lesions in the nervous system. Vet. Parasitol. 143 (2007) 174-181
4. Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 27 (1999) 573-580
5. Brisse S., Henriksson J., Barnabé C., Douzery E.J.P., Berkvens D., Serrano M., De Carvalho M.R.C., Buck G.A., Dujardin J., and Tibayrenc M. Evidence for genetic exchange and hybridization in Trypanosoma cruzi based on nucleotide sequences and molecular karyotype. Infect. Genet. Evol. 2 (2003) 173-183
6. Catley A., Irungu P., Simiyu K., Dadye J., Mwakio W., Kiragu J., and Nyamwaro S.O. Participatory investigations of bovine trypanosomiasis in Tana River District, Kenya. Med. Vet. Entomol. 16 (2002) 55-66
7. Cherenet T., Sani R.A., Speybroeck N., Panandam J.M., Nadzr S., and Van den Bossche P. A comparative longitudinal study of bovine trypanosomiasis in tsetse-free and tsetse-infested zones of the Amhara region, northwest Ethiopia. Vet. Parasitol. 140 (2006) 251-258
8. Cortez A.P., Ventura R.M., Rodrigues A.C., Batista J.S., Paiva F., Añez N., Machado R.Z., Gibson W.C., and Teixeira M.M.G. The taxonomic and phylogenetic relationships of Trypanosoma vivax from South America and Africa. Parasitology 133 (2006) 159-169
9. de Freitas J.M., Augusto-Pinto L., Pimenta J.R., Bastos-Rodrigues L., Gonçalves V.F., Teixeira S.M.R., Chiari E., Junqueira A.C.V., Fernandes O., Macedo A.M., Machado C.R., and Pena S.D.J. Ancestral genomes, sex, and the population structure of Trypanosoma cruzi. PLoS Pathog. 2 (2006) 226-235
10. De Meeûs T., Lehmann L., and Balloux F. Molecular epidemiology of clonal diploids: a quick overview and a short diy (do it yourself) notice. Infect. Genet. Evol. 6 (2006) 163-170
11. Delafosse A., Thébaud E., Desquesnes M., and Michaux Y. Epidemiology of Trypanosoma vivax infection in cattle in the tsetse free area of Lake Chad. Prev. Vet. Med. 74 (2006) 108-119
12. Desquesnes M., and Dia M.L. Mechanical transmission of Trypanosoma vivax in cattle by the African tabanid Atylotus fuscipes. Vet. Parasitol. 119 (2004) 9-19
13. Dirie M.F., Murphy N.B., and Gardiner P.R. DNA fingerprinting of Trypanosoma vivax isolates rapidly identifies intraspecific relationships. J. Eukaryot. Microbiol. 40 (1993) 132-134
14. El-Sayed N.M., Myler P.J., Bartholomeu D.C., Nilsson D., Aggarwal G., Tran A., Ghedin E., Worthey E.A., Delcher A.L., Blandin G., Westenberger S.J., Caler E., Cerqueira G.C., Branche C., Haas B., Anupama A., Arner E., Aslund L., Attipoe P., Bontempi E., Bringaud F., Burton P., Cadag E., Campbell D.A., Carrington M., Crabtree J., Darban H., da Silveira J.F., de Jong P., Edwards K., Englund P.T., Fazelina G., Feldblyum T., Ferella M., Frasch A.C., Gull K., Horn D., Hou L., Huang Y., Kindlund E., Klingbeil M., Kluge S., Koo H., Lacerda D., Levin M.J., Lorenzi H., Louie T., Machado C.R., McCulloch R., McKenna A., Mizuno Y., Mottram J.C., Nelson S., Ochaya S., Osoegawa K., Pai G., Parsons M., Pentony M., Pettersson U., Pop M., Ramirez J.L., Rinta J., Robertson L., Salzberg S.L., Sanchez D.O., Seyler A., Sharma R., Shetty J., Simpson A.J., Sisk E., Tammi M.T., Tarleton R., Teixeira S., Van Aken S., Vogt C., Ward P.N., Wickstead B., Wortman J., White O., Fraser C.M., Stuart K.D., and Andersson B. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309 (2005) 409-415
15. Fasogbon A.I., Knowles G., and Gardiner P.R. A comparison of the isoenzymes of Trypanosoma (Duttonella) vivax isolates from East and West Africa. Int. J. Parasitol. 20 (1990) 389-394
16. Faye D., Pereira de Almeida P.J., Goossens B., Osaer S., Ndao M., Berkvens D., Speybroeck N., Nieberding F., and Geerts S. Prevalence and incidence of trypanosomosis in horses and donkeys in The Gambia. Vet. Parasitol. 101 (2001) 101-114
17. Gardiner P.R. Recent studies of the biology of Trypanosoma vivax. Adv. Parasitol. 28 (1989) 229-317
18. Gardiner P.R., and Wilson A.J. Trypanosoma (Duttonella) vivax. Parasitol. Today 3 (1987) 49-52
19. Gashumba J.K., Baker R.D., and Godfrey D.G. Trypanosoma congolense: the distribution of enzymic variants in East and West Africa. Parasitology 96 (1988) 475-486
20. Gaunt M.W., Yeo M., Frame I.A., Stothard J.R., Carrasco H.J., Taylor M.C., Mena S.S., Veazey P., Miles G.A.J., Acosta N., de Arias A.R., and Miles M.A. Mechanism of genetic exchange in American trypanosomes. Nature 421 (2003) 936-939
21. Gibson W. Resolution of the species problem in African trypanosomes. Int. J. Parasitol. 37 (2007) 829-838
22. Haas S., Vingron M., Poustka A., and Wiemann S. Primer design for large scale sequencing. Nucleic Acids Res. 26 (1998) 3006-3012
23. Halkett F., Simon J., and Balloux F. Tackling the population genetics of clonal and partially clonal organisms. Trends Ecol. Evol. 20 (2005) 194-201
24. Hoare C. The Trypanosomes of Mammals (1972), Blackwell Scientific Publications, Oxford and Edinburgh
25. Jamonneau V., Barnabé C., Koffi M., Sané B., Cuny G., and Solano P. Identification of Trypanosoma brucei circulating in a sleeping sickness focus in Côte d'Ivoire: assessment of genotype selection by the isolation method. Infect. Genet. Evol. 3 (2003) 143-149
26. Jones T.W., and Dávila A.M. Trypanosoma vivax - out of Africa. Trends Parasitol. 17 (2001) 99-101
27. Kalu A.U., Oboegbulem S.I., and Uzoukwu M. Trypanosomosis in small ruminants maintained by low riverine tsetse population in central Nigeria. Small Rumin. Res. 40 (2001) 109-115
28. Kilgour V., and Godfrey D.G. The persistence in the field of two characteristic isoenzyme patterns in Nigerian Trypanosoma vivax. Ann. Trop. Med. Parasitol. 71 (1977) 387-389
29. Kilgour V., Godfrey D.G., and Na'isa B.K. Isoenzymes of two aminotransferases among Trypanosoma vivax in Nigerian cattle. Ann. Trop. Med. Parasitol. 69 (1975) 329-335
30. Koffi M., De Meeûs T., Bucheton B., Solano P., Camara M., Kaba D., Cuny G., Ayala F.J., and Jamonneau V. Population genetics of Trypanosoma brucei gambiense, the agent of sleeping sickness in Western Africa. Proc. Natl. Acad. Sci. USA 106 (2009) 209-214
31. Koffi M., Solano P., Barnabé C., de Meeûs T., Bucheton B., Cuny G., and Jamonneau V. Genetic characterisation of Trypanosoma brucei s.l. using microsatellite typing: new perspectives for the molecular epidemiology of human African trypanosomiasis. Infect. Genet. Evol. 7 (2007) 675-684
32. Lai D., Hashimi H., Lun Z., Ayala F.J., and Lukes J. Adaptations of Trypanosoma brucei to gradual loss of kinetoplast DNA: Trypanosoma equiperdum and Trypanosoma evansi are petite mutants of T. brucei. Proc. Natl. Acad. Sci. USA 105 (2008) 1999-2004
33. MacLeod A., Tait A., and Turner C.M. The population genetics of Trypanosoma brucei and the origin of human infectivity. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356 (2001) 1035-1044
34. MacLeod A., Turner C.M., and Tait A. A high level of mixed Trypanosoma brucei infections in tsetse flies detected by three hypervariable minisatellites. Mol. Biochem. Parasitol. 102 (1999) 237-248
35. MacLeod A., Tweedie A., McLellan S., Hope M., Taylor S., Cooper A., Sweeney L., Turner C.M.R., and Tait A. Allelic segregation and independent assortment in T. brucei crosses: proof that the genetic system is Mendelian and involves meiosis. Mol. Biochem. Parasitol. 143 (2005) 12-19
36. MacLeod A., Tweedie A., Welburn S.C., Maudlin I., Turner C.M., and Tait A. Minisatellite marker analysis of Trypanosoma brucei: reconciliation of clonal, panmictic, and epidemic population genetic structures. Proc. Natl. Acad. Sci. USA 97 (2000) 13442-13447
37. Magona J.W., Walubengo J., and Odimin J.T. Acute haemorrhagic syndrome of bovine trypanosomosis in Uganda. Acta Trop. 107 (2008) 186-191
38. Masiga D.K., Smyth A.J., Hayes P., Bromidge T.J., and Gibson W.C. Sensitive detection of trypanosomes in tsetse flies by DNA amplification. Int. J. Parasitol. 22 (1992) 909-918
39. Maynard-Smith J., Smith N.H., O'Rourke M., and Spratt B.G. How clonal are bacteria?. Proc. Natl. Acad. Sci. USA 90 (1993) 4384-4388
40. McNamara J.J., Bailey J.W., Smith D.H., Wakhooli S., and Godfrey D.G. Isolation of Trypanosoma brucei gambiense from northern Uganda: evaluation of the kit for in vitro isolation (KIVI) in an epidemic focus. Trans. R. Soc. Trop. Med. Hyg. 89 (1995) 388-389
41. Morrison L.J., McCormack G., Sweeney L., Likeufack A.C.L., Truc P., Turner C.M., Tait A., and MacLeod A. Use of multiple displacement amplification to increase the detection and genotyping of Trypanosoma species samples immobilized on FTA filters. Am. J. Trop. Med. Hyg. 76 (2007) 1132-1137
42. Morrison L.J., Tait A., McCormack G., Sweeney L., Black A., Truc P., Likeufack A.C.L., Turner C.M., and MacLeod A. Trypanosoma brucei gambiense type 1 populations from human patients are clonal and display geographical genetic differentiation. Infect. Genet. Evol. 8 (2008) 847-854
43. Morrison L.J., Tweedie A., Black A., Pinchbeck G., Christley R.M., Schoenefeld A., Hertz-Fowler C., MacLeod A., Turner C.M.R., and Tait A. Discovery of mating in the major African livestock pathogen Trypanosoma congolense. PLOS One 4 (2009) e5564
44. Njiokou F., Simo G., Nkinin S.W., Laveissière C., and Herder S. Infection rate of Trypanosoma brucei s.l., T. vivax, T. congolense "forest type", and T. simiae in small wild vertebrates in south Cameroon. Acta Trop. 92 (2004) 139-146
45. Osório A.L.A.R., Madruga C.R., Desquesnes M., Soares C.O., Ribeiro L.R.R., and Costa S.C.G.D. Trypanosoma (Duttonella) vivax: its biology, epidemiology, pathogenesis, and introduction in the New World - a review. Mem. Inst. Oswaldo Cruz 103 (2008) 1-13
46. Page R.D. Treeview: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12 (1996) 357-358
47. Peakall R., and Smouse P.E. Genalex 6: genetic analysis in excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6 (2006) 288-295
48. Pinchbeck G.L., Morrison L.J., Tait A., Langford J., Meehan L., Jallow S., Jallow J., Jallow A., and Christley R.M. Trypanosomosis in The Gambia: prevalence in working horses and donkeys detected by whole genome amplification and PCR, and evidence for interactions between trypanosome species. BMC Vet. Res. 4 (2008) 7
49. Ramesh M.A., Malik S., and Logsdon J.M.J. A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Curr. Biol. 15 (2005) 185-191
50. Rodrigues A.C., Neves L., Garcia H.A., Viola L.B., Marcili A., Da Silva F.M., Sigauque I., Batista J.S., Paiva F., and Teixeira M.M.G. Phylogenetic analysis of Trypanosoma vivax supports the separation of South American/West African from East African isolates and a new T. vivax-like genotype infecting a nyala antelope from Mozambique. Parasitology 135 (2008) 1317-1328
51. Schurko A.M., and Logsdon J.M.J. Using a meiosis detection toolkit to investigate ancient asexual "scandals" and the evolution of sex. Bioessays 30 (2008) 579-589
52. Shaw AP. Economics of African trypanosomiasis. In: Maudlin I., Holmes P., and Miles M. (Eds). The Trypanosomiases (2004), CABI Publishing, Wallingford, UK
53. Silva R.A., Morales G., Eulert E., Montenegro A., and Ybañez R. Outbreaks of trypanosomosis due to Trypanosoma vivax in cattle in Bolivia. Vet. Parasitol. 76 (1998) 153-157
54. Simo G., Cuny G., Demonchy R., and Herder S. Trypanosoma brucei gambiense: study of population genetic structure of Central African stocks using amplified fragment length polymorphism (AFLP). Exp. Parasitol. 118 (2007) 172-180
55. Sinshaw A., Abebe G., Desquesnes M., and Yoni W. Biting flies and Trypanosoma vivax infection in three highland districts bordering Lake Tana, Ethiopia. Vet. Parasitol. 142 (2006) 35-46
56. Stenberg P., Lundmark M., and Saura A. MLGsim: a program for detecting clones using a simulation approach. Mol. Ecol. Notes 3 (2003) 329-331
57. Stevens J.R., Noyes H.A., Dover G.A., and Gibson W.C. The ancient and divergent origins of the human pathogenic trypanosomes, Trypanosoma brucei and T. cruzi. Parasitology 118 (1999) 107-116
58. Taylor K.A., and Mertens B. Immune response of cattle infected with African trypanosomes. Mem. Inst. Oswaldo Cruz 94 (1999) 239-244
59. Tibayrenc M., Kjellberg F., and Ayala F.J. A clonal theory of parasitic protozoa: the population structures of Entamoeba, Giardia, Leishmania, Naegleria, Plasmodium, Trichomonas, and Trypanosoma and their medical and taxonomical consequences. Proc. Natl. Acad. Sci. USA 87 (1990) 2414-2418
60. Tibayrenc M., Kjellberg F., Arnaud J., Oury B., Brenière S.F., Dardé M.L., and Ayala F.J. Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc. Natl. Acad. Sci. USA 88 (1991) 5129-5133
61. Turner C.M., Sternberg J., Buchanan N., Smith E., Hide G., and Tait A. Evidence that the mechanism of gene exchange in Trypanosoma brucei involves meiosis and syngamy. Parasitology 101 (1990) 377-386
62. Waiswa C., and Katunguka-Rwakishaya E. Bovine trypanosomiasis in south-western Uganda: packed-cell volumes and prevalences of infection in the cattle. Ann. Trop. Med. Parasitol. 98 (2004) 21-27
63. Westenberger S.J., Barnabé C., Campbell D.A., and Sturm N.R. Two hybridization events define the population structure of Trypanosoma cruzi. Genetics 171 (2005) 527-543
64. Young C.J., and Godfrey D.G. Enzyme polymorphism and the distribution of Trypanosoma congolense isolates. Ann. Trop. Med. Parasitol. 77 (1983) 467-481