Variation in the structure of Toxoplasma gondii and the roles of selfing, drift, and epistatic selection in maintaining linkage disequilibria

Infection, Genetics and Evolution

Volumn 4, Issue 2, 2004, Pages 107-114

  Lehmann, Tovi ^a   Graham, Douglas H ^a,e   Dahl, Erica R ^a   Bahia Oliveira, Lilian M G ^b   Gennari, S M ^c   Dubey, J P ^d  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b UNIVERSIDADE ESTADUAL DO NORTE FLUMINENSE DARCY RIBEIRO   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d AGRICULTURAL RESEARCH SERVICE   (United States)

^e GRAND VALLEY STATE UNIVERSITY   (United States)

Author keywords

Clonal structure; Linkage disequilibrium; Microsatellite; Molecular epidemiology; Sex; Strain typing; Toxoplasma; Zoonosis

Indexed keywords

ARTICLE; BRAZIL; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENE STRUCTURE; GENETIC DRIFT; GENETIC EPISTASIS; GENETIC HETEROGENEITY; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHIC DISTRIBUTION; HOST PATHOGEN INTERACTION; LIFE CYCLE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; REPRODUCTION; SELFING; SPECIES HABITAT; TOXOPLASMA GONDII; UNITED STATES;

ALLELES; ANIMALS; ANIMALS, DOMESTIC; EPISTASIS, GENETIC; GENETIC DRIFT; HETEROZYGOTE; LINKAGE DISEQUILIBRIUM; POLYMORPHISM, GENETIC; TOXOPLASMA; VARIATION (GENETICS);

FELIS CATUS; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 2442618856     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2004.01.007     Document Type: Article

References (54)

1. Ajzenberg D. Banuls A.L. Tibayrenc M. Darde M.L. Microsatellite analysis of Toxoplasma gondii shows considerable polymorphism structured into two main clonal groups Int. J. Parasitol. 32 2002 27-38
2. Anderson T.J. Haubold B. Williams J.T. Estrada-Franco J.G. Richardson L. Mollinedo R. Bockarie M. Mokili J. Mharakurwa S. French N. Whitworth J. Velez I.D. Brockman A.H. Nosten F. Ferreira M.U. Day K.P. Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum Mol. Biol. Evol. 17 2000 1467-1482
3. Aspinall T.V. Guy E.C. Roberts K.E. Joynson D.H. Hyde J.E. Sims P.F. Molecular evidence for multiple Toxoplasma gondii infections in individual patients in England and Wales: public health implications Int. J. Parasitol. 33 2003 97-103
4. Aspinall T.V. Marlee D. Hyde J.E. Sims P.F. Prevalence of Toxoplasma gondii in commercial meat products as monitored by polymerase chain reaction-food for thought? Int. J. Parasitol. 32 2002 1193-1199
5. Bahia-Oliveira L.M. Jones J.L. Azevedo-Silva J. Alves C.C. Orefice F. Addiss D.G. Highly endemic, waterborne toxoplasmosis in north Rio de Janeiro state Brazil Emerg. Infect. Dis. 9 2003 55-62
6. Belanger F. Derouin F. Grangeot-Keros L. Meyer L. Incidence and risk factors of toxoplasmosis in a cohort of human immunodeficiency virus-infected patients: 1988-1995. HEMOCO and SEROCO Study Groups Clin. Infect. Dis. 28 1999 575-581
7. Blackston C.R. Dubey J.P. Dotson E. Su C. Thulliez P. Sibley D. Lehmann T. High-resolution typing of Toxoplasma gondii using microsatellite loci J. Parasitol. 87 2001 1472-1475
8. Carme B. Aznar C. Motard A. Demar M. de Thoisy B. Serologic survey of Toxoplasma gondii in noncarnivorous free-ranging neotropical mammals in French Guiana Vector Borne Zoonotic Dis. 2 2002 11-17
9. da Silva D.S. Bahia-Oliveira L.M. Shen S.K. Kwok O.C. Lehman T. Dubey J.P. Prevalence of Toxoplasma gondii in chickens from an area in southern Brazil highly endemic to humans J. Parasitol. 89 2003 394-396
10. Darde M.L. Biodiversity in Toxoplasma gondii Curr. Top. Microbiol. Immunol. 219 1996 27-41
11. Darde M.L. Bouteille B. Pestre-Alexandre M. Isoenzyme analysis of 35 Toxoplasma gondii isolates and the biological and epidemiological implications J. Parasitol. 78 1992 786-794
12. Dubey J.P. Toxoplasma gondii oocyst survival under defined temperatures J. Parasitol. 84 1998 862-865
13. Dubey, J.P., Beattie, C.P., 1988. Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, FL.
14. Dubey J.P. Frenkel J.K. Feline toxoplasmosis from acutely infected mice and the development of Toxoplasma cysts J. Protozool. 23 1976 537-546
15. Dubey J.P. Graham D.H. Blackston C.R. Lehmann T. Gennari S.M. Ragozo A.M. Nishi S.M. Shen S.K. Kwok O.C. Hill D.E. Thulliez P. Biological and genetic characterisation of Toxoplasma gondii isolates from chickens (Gallus domesticus) from Sao Paulo, Brazil: unexpected findings Int. J. Parasitol. 32 2002 99-105
16. Dubey J.P. Graham D.H. Dahl E. Sreekumar C. Lehmann T. Davis M.F. Morishita T.Y. Toxoplasma gondii isolates from free-ranging chickens from the United States J. Parasitol. 89 2003a 1060-1062
17. Dubey J.P. Navarro I.T. Graham D.H. Dahl E. Freire R.L. Prudencio L.B. Sreekumar C. Vianna M.C. Lehmann T. Characterization of Toxoplasma gondii isolates from free range chickens from Parana, Brazil Vet. Parasitol. 117 2003 229-234
18. Dubey J.P. Thulliez P. Powell E.C. Toxoplasma gondii in Iowa sows: comparison of antibody titers to isolation of T. gondii by bioassays in mice and cats J. Parasitol. 81 1995 48-53
19. Elphick, J., 1995. The Atlas of Bird Migration. Random House, New York.
20. Estoup A. Garnery L. Solignac M. Cornuet J.M. Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models Genetics 140 1995 679-695
21. Grigg M.E. Bonnefoy S. Hehl A.B. Suzuki Y. Boothroyd J.C. Success and virulence in Toxoplasma as the result of sexual recombination between two distinct ancestries Science 294 2001 161-165
22. Holm S. A simple sequentially rejective multiple test procedure Scand. J. Stat. 6 1979 65-70
23. Howe D.K. Honore S. Derouin F. Sibley L.D. Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis J. Clin. Microbiol. 35 1997 1411-1414
24. Howe D.K. Sibley L.D. Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease J. Infect. Dis. 172 1995 1561-1566
25. Jones J.L. Kruszon-Moran D. Wilson M. McQuillan G. Navin T. McAuley J.B. Toxoplasma gondii infection in the United States: seroprevalence and risk factors Am. J. Epidemiol. 154 2001 357-365
26. Lan R. Reeves P.R. When does a clone deserve a name? A perspective on bacterial species based on population genetics Trends Microbiol. 9 2001 419-424
27. Langley C.H. Tobari Y.N. Kojima K.I. Linkage disequilibrium in natural populations of Drosophila melanogaster Genetics 78 1974 921-936
28. Lehmann T. Blackston C.R. Parmley S.F. Remington J.S. Dubey J.P. Strain typing of Toxoplasma gondii: comparison of antigen-coding and housekeeping genes J. Parasitol. 86 2000 960-971
29. Lehmann T. Hawley W.A. Collins F.H. An evaluation of evolutionary constraints on microsatellite loci using null alleles Genetics 144 1996 1155-1163
30. Lehmann T. Hawley W.A. Grebert H. Collins F.H. The effective population size of Anopheles gambiae in Kenya: implications for population structure Mol. Biol. E 15 1998 264-276
31. Lenski R.E. Assessing the genetic structure of microbial populations Proc. Natl. Acad. Sci. U.S.A. 90 1993 4334-4336
32. Lewontin R.C. The interaction of selection and linkage I Genetics 49 1964 49-67
33. Lindsay D.S. Blagburn B.L. Dubey J.P. Survival of nonsporulated Toxoplasma gondii oocysts under refrigerator conditions Vet. Parasitol. 103 2002 309-313
34. Mantel N. The detection of disease clustering and a generalized regression approach Cancer Res. 27 1967 209-220
35. Miller M.A. Gardner I.A. Kreuder C. Paradies D.M. Worcester K.R. Jessup D.A. Dodd E. Harris M.D. Ames J.A. Packham A.E. Conrad P.A. Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis) Int. J. Parasitol. 32 2002 997-1006
36. Mondragon R. Howe D.K. Dubey J.P. Sibley L.D. Genotypic analysis of Toxoplasma gondii isolates from pigs J. Parasitol. 84 1998 639-641
37. Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.
38. Pfefferkorn L.C. Pfefferkorn E.R. Toxoplasma gondii: genetic recombination between drug resistant mutants Exp. Parasitol. 50 1980 305-316
39. Raymond M. Rousset F. GENEPOP (Version 1.2) population genetics software for exact tests and ecumenicism J. Hered. 86 1995a 248-249
40. Reynolds, H.T., 1984. Analysis of Nominal Data. Sage Publications, Beverly Hills, CA, USA.
41. SAS Institute Inc. (1999) SAS® Procedures Guide, Version 8 (SAS Institute: Cary, NC).
42. Sibley L.D. Boothroyd J.C. Virulent strains of Toxoplasma gondii comprise a single clonal lineage Nature 359 1992 82-85
43. Silveira C. Belfort R. Jr. Muccioli C. Abreu M.T. Martins M.C. Victora C. Nussenblatt R.B. Holland G.N. A follow-up study of Toxoplasma gondii infection in southern Brazil Am. J. Ophthalmol. 131 2001 351-354
44. Smith J.M. Smith N.H. O'Rourke M. Spratt B.G. How clonal are bacteria? Proc. Natl. Acad Sci. U.S.A. 90 1993 4384-4388
45. Souza V. Nguyen T.T. Hudson R.R. Pinero D. Lenski R.E. Hierarchical analysis of linkage disequilibrium in Rhizobium populations: evidence for sex? Proc. Natl. Acad. Sci. U.S.A. 89 1992 8389-8393
46. Spratt B.G. Hanage W.P. Feil E.J. The relative contributions of recombination and point mutation to the diversification of bacterial clones Curr. Opin. Microbiol. 4 2001 602-606
47. Su C. Howe D.K. Dubey J.P. Ajioka J.W. Sibley L.D. Identification of quantitative trait loci controlling acute virulence in Toxoplasma gondii Proc. Natl. Acad. Sci. U.S.A. 99 2002 10753-10758
48. Tibayrenc M. Ayala F. The clonal theory of parasitic protozoa: 12 years on Trends Parasitol. 18 2002 405
49. Tibayrenc M. Kjellberg F. Arnaud J. Oury B. Breniere S.F. Darde M.L. Ayala F.J. Are eukaryotic microorganisms clonal or sexual? A population genetics vantage Proc. Natl. Acad. Sci. U.S.A. 88 1991 5129-5133
50. Wallace B. Coadaptation revisited J. Hered. 82 1991 89-95
51. Weir B.S. Cockerham C.C. Estimating F-statistics for the analysis of population sructure Evolution 38 1984 1358-1370
52. Zapata C. The D′ measure of overall gametic disequilibrium between pairs of multiallelic loci Evolut. Int. J. Org. Evolut. 54 2000 1809-1812
53. Zapata C. Carollo C. Rodriguez S. Sampling variance and distribution of the D′ measure of overall gametic disequilibrium between multiallelic loci Ann. Hum. Genet. 65 2001 395-406
54. Zarnke R.L. Dubey J.P. Kwok O.C. Ver Hoef J.M. Serologic survey for Toxoplasma gondii in selected wildlife species from Alaska J. Wildl. Dis. 36 2000 219-224