Genetic structure of Schstosoma mansoni in western Kenya: The effects of geography and host sharing

International Journal for Parasitology

Volumn 39, Issue 12, 2009, Pages 1353-1362

  Steinauer, M L ^a   Hanelt, B ^a   Agola, L E ^b   Mkoji, G M ^b   Loker, E S ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

Author keywords

Coinfection; Competition; Genetic structure; Host sharing; Kenya; Kin selection; Lake Victoria; Schistosoma mansoni

Indexed keywords

ANTIPROTOZOAL AGENT;

BIOMARKER; CLONE; COMPETITION (ECOLOGY); GENE FLOW; GENETIC STRUCTURE; GENOTYPE; KIN SELECTION; PARASITE; POPULATION GENETICS; POPULATION STRUCTURE; RELATEDNESS;

ANTIBIOTIC RESISTANCE; ARTICLE; CERCARIA; CERCARIA (TREMATODE LARVA); COMPETITION; CONTROLLED STUDY; GENE FLOW; GENE STRUCTURE; GENETIC VARIABILITY; GENOTYPE; GEOGRAPHY; HOST; HYPOTHESIS; KENYA; KIN SELECTION; LAKE; MICROSATELLITE MARKER; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE TRANSMISSION; PARASITE VIRULENCE; POPULATION STRUCTURE; PROTOZOAL GENETICS; REPRODUCTION; SCHISTOSOMA MANSONI; SNAIL;

ANIMALS; FEMALE; FRESH WATER; GENETIC MARKERS; HOST-PARASITE INTERACTIONS; HUMANS; KENYA; MALE; MICROSATELLITE REPEATS; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS MANSONI; SNAILS; VIRULENCE;

AFRICA; EAST AFRICA; KENYA; SUB-SAHARAN AFRICA;

GASTROPODA; SCHISTOSOMA MANSONI;

EID: 68049148359     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2009.04.010     Document Type: Article

References (72)

1. Agola L.E., Mburu D.N., DeJong R.J., Mungai B.N., Muluvi G.M., Njagi E.N.M., Loker E.S., and Mkoji G.M. Microsatellite typing reveals strong genetic structure of Schistosoma mansoni from localities in Kenya. Infect. Genet. Evol. 6 (2006) 484-490
2. Archie E.A., Luikart G., and Ezenwa V.O. Infecting epidemiology with genetics: a new frontier in disease ecology. Trends in Ecology & Evolution 24 (2009) 21-30
3. Black C.L., Steinauer M.L., Mwinzi P.N.M., Secor W.E., Karanja D.M.S., and Colley D.G. Impact of intense, longitudinal retreatment with praziquantel on cure rates of schistosomiasis mansoni in a cohort of occupationally exposed adults in western Kenya. Trop. Med. Int. Health 14 (2009) 1-8
4. Blouin M.S., Yowell C.A., Courtney C.H., and Dame J.B. Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141 (1995) 1007-1014
5. Blouin M.S., Liu J., and Berry R.E. Life cycle variation and the genetic structure of nematode populations. Heredity 83 (1999) 253-259
6. Born C., Hardy O.J., Chevallier M.H., Ossari S., Atteke C., Wickings E.J., and Hosseart-McKey M. Small-scale spatial genetic structure in the Central African rainforest tree species Aucoumea klaineana: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation. Mol. Ecol. 17 (2008) 2041-2050
7. Bremermann H.J., and Pickering J. A game-theoretical model of parasite virulence. J. Theor. Biol. 100 (1983) 411-426
8. Brown S.P., Hochberg M.E., and Grenfell B.T. Does multiple infection select for raised virulence?. Trends Microbiol. 10 (2002) 401-405
9. Buckling A., and Hodgson D.J. Short-term rates of parasite evolution predict the evolution of host diversity. J. Evol. Biol. 20 (2007) 1682-1688
10. Buckling A., and Brockhurst M.A. Kin selection and the evolution of virulence. Heredity 100 (2008) 484-488
11. Chao L., Hanley K.A., Burch C.L., Dahlberg C., and Turner P.E. Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. Q Rev. Biol. 75 (2000) 261-275
12. Criscione C.D., and Blouin M.S. Life cycles shape parasite evolution: comparative population genetics of salmon and trematodes. Evolution 58 (2004) 198-202
13. Criscione C.D., Poulin R., and Blouin M.S. Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol. Ecol. 14 (2005) 2247-2257
14. Criscione C.D., and Blouin M.S. Minimal selfing, few clones, and no among-host genetic structure in a hermaphroditic parasite with asexual larval propagation. Evolution 60 (2006) 553-562
15. Curtis J., Sorensen R.E., Page L.K., and Minchella D.J. Microsatellite loci in the human blood fluke Schistosoma mansoni and their utility for other schistosome species. Mol. Ecol. Notes 1 (2001) 143-145
16. Curtis J., Sorensen R.E., and Minchella D.J. Schistosome genetic diversity: the implications of population structure as detected with microsatellite markers. Parasitology 125 (2002) S51-S59
17. Davies C.M., Webster J.P., and Woolhouse M.E.J. Trade-offs in the evolution of virulence in an indirectly transmitted macroparasite. Proc. R. Soc. Lond. B Biol. Sci. 268 (2001) 251-257
18. Davies C.M., Fairbrother E., and Webster J.P. Mixed strain schistosome infections of snails and the evolution of parasite virulence. Parasitology 124 (2002) 31-38
19. Feng Z.L., Curtis J., and Minchella D.J. The influence of drug treatment on the maintenance of schistosome genetic diversity. Journal of Mathematical Biology 43 (2001) 52-68
20. Frank S.A. A kin selection model for the evolution of virulence. Proc. R. Soc. Lond. B Biol. Sci. 250 (1992) 195-197
21. Frank S.A. Models of parasite virulence. Q Rev. Biol. 71 (1996) 37-78
22. Fulford A.J.C., Butterworth A.E., Ouma J.H., and Sturrock R.F. A statistical approach to schistosome population dynamics and estimation of the life span of Schistosoma mansoni in man. Parasitology 110 (1995) 307-316
23. Geerts S., and Gryseels B. Drug resistance in human helminths: current situation and lessons from livestock. Clin. Microbiol. Rev. 13 (2000) 207-222
24. Goudet, J., 2001. Posting date. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from: .
25. Gower C.M., and Webster J.P. Intraspecific competition and the evolution of virulence in a parasitic trematode. Evolution 59 (2005) 544-553
26. Gower C.M., Shrivastava J., Lamberton P.H.L., Rollinson D., Webster B.L., Emery A., Kabatereine N.B., and Webster J.P. Development and application of an ethically and epidemiologically advantageous assay for the multi-locus microsatellite analysis of Schistosoma mansoni. Parasitology 134 (2007) 523-536
27. Hamilton W.D. Altruism and related phenomena, mainly in social insects. Annu. Rev. Ecol. Syst. 3 (1972) 193-232
28. Handzel T., Karanja D.M.S., Addiss D.G., Hightower A.W., Rosen D.H., Colley D.G., Andove J., Slutsker L., and Secor W.E. Geographic distribution of schistosomiasis and soil-transmitted helminths in Western Kenya: implications for anthelminthic mass treatment. Am. J. Trop. Med. Hyg. 69 (2003) 318-323
29. Hardy O.J., and Vekemans X. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes 2 (2002) 618-620
30. Huyse T., Poulin R., and Theron A. Speciation in parasites: a population genetics approach. Trends Parasitol. 21 (2005) 469-475
31. Jager I., and Schjørring S. Multiple infections: relatedness and time between infections affect the establishment and growth of the cestode Schistocephalus solidus in its stickleback host. Evolution 60 (2006) 616-622
32. Kalinowski S.T., Wagner A.P., and Taper M.L. ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Mol. Ecol. Notes 6 (2006) 576-579
33. Karanja D.M.S., Hightower A.W., Colley D.G., Mwinzi P.N.M., Galil K., Andove J., and Secor W.E. Resistance to reinfection with Schistosoma mansoni in occupationally exposed adults and effect of HIV-1 co-infection on susceptibility to schistosomiasis: a longitudinal study. Lancet 360 (2002) 592-596
34. Kardorff R., Gabone R.M., Mugashe C., Obiga D., Ramarokoto C.E., Mahlert C., Spannbrucker N., Lang A., Gunzler V., Gryseels B., Ehrich J.H.H., and Doehring E. Schistosoma mansoni related morbidity on Ukerewe Island, Tanzania: clinical, ultrasonographical and biochemical parameters. Trop. Med. Int. Health 2 (1997) 230-239
35. Keeney D.B., Waters J.M., and Poulin R. Diversity of trematode genetic clones within amphipods and the timing of same-clone infections. Int. J. Parasitol. 37 (2007) 351-357
36. King C.H., Dickman K., and Tisch D.J. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365 (2005) 1561-1569
37. Leathwick D.M., Miller C.M., Atkinson D.S., Haack N.A., Waghorn T.S., and Oliver A.M. Managing anthelmintic resistance: untreated adult ewes as a source of unselected parasites, and their role in reducing parasite populations. New Zealand Veterinary Journal 56 (2008) 184-195
38. Levin S., and Pimentel D. Selection of intermediate rates of increase in parasite-host systems. American Naturalist 117 (1981) 308-315
39. Li G., and Hedgecock D. Genetic heterogeneity, detected by PCR-SSCP, among samples of larval Pacific oysters (Crassostrea gigas) supports the hypothesis of large variance in reproductive success. Canadian Journal of Fisheries and Aquatic Sciences 55 (1998) 1025-1033
40. Loiselle B.A., Sork V.L., Nason J., and Graham C. Spatial genetic-structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am. J. Bot. 82 (1995) 1420-1425
41. Lotz J.M., Bush A.O., and Font W.F. Recruitment-driven, spatially discontinuous communities: a null model for transferred patterns in target communities of intestinal helminths. J. Parasitol. 81 (1995) 12-24
42. Lynch M., and Ritland K. Estimation of pairwise relatedness with molecular markers. Genetics 152 (1999) 1753-1766
43. May R.M., and Nowak M.A. Coinfection and the evolution of parasite virulence. Proc. R. Soc. Lond. B Biol. Sci. 261 (1995) 209-215
44. McCoy K.D., Boulinier T., Tirard C., and Michalakis Y. Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57 (2003) 288-296
45. Meirmans P.G. Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60 (2006) 2399-2402
46. Nei M. Molecular Evolutionary Genetics (1987), Columbia University Press, New York
47. Pritchard J.K., Stephens M., and Donnelly P. Inference of population structure using multilocus genotype data. Genetics 155 (2000) 945-959
48. Prugnolle F., De Meeus T., Durand P., Sire C., and Theron A. Sex-specific genetic structure in Schistosoma mansoni: evolutionary and epidemiological implications. Mol. Ecol. 11 (2002) 1231-1238
49. Queller D.C., and Goodnight K.F. Estimating relatedness using genetic markers. Evolution 43 (1989) 258-275
50. Rice W.R. Analyzing tables of statistics tests. Evolution 43 (1989) 223-225
51. Rousset F. Genepop™007: a complete re-implementation of the genepop software for Windows and Linux. Mol. Ecol. Resources 8 (2008) 103-106
52. Schjørring S., and Koella J.C. Sub-lethal effects of pathogens can lead to the evolution of lower virulence in multiple infections. Proc. R. Soc. Lond. B Biol. Sci. 270 (2003) 189-193
53. Shrivastava J., Gower C.M., Balolong E., Wang T.P., Qian B.Z., and Webster J.P. Population genetics of multi-host parasites: the case for molecular epidemiological studies of Schistosoma japonicum using larval stages from naturally infected hosts. Parasitology 131 (2005) 617-626
54. Silva L., Liu S., and Blanton R.E. Microsatellite analysis of pooled Schistosoma mansoni DNA: an approach for studies of parasite populations. Parasitology 132 (2006) 331-338
55. Sissay M.M., Asefa A., Uggla A., and Waller P.J. Anthelmintic resistance of nematode parasites of small ruminants in eastern Ethiopia: exploitation of refugia to restore anthelmintic efficacy. Veterinary Parasitology 135 (2006) 337-346
56. Smithers S.R., and Terry R.S. The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55 (1965) 695-700
57. Steinauer M.L., Agola L.E., Mwangi I.N., Mkoji G.M., and Loker E.S. Molecular epidemiology of Schistosoma mansoni: a robust, high-throughput method to assess multiple microsatellite markers from individual miracidia. Infect. Genet. Evol. 8 (2008) 68-73
58. Steinauer M.L., Hanelt B., Mwangi I.N., Maina G.M., Agola E.L., Kinuthia J.M., Mutuku M.W., Mungai B.N., Wilson W.D., Mkoji G.M., and Loker E.S. Introgressive hybridization of human and rodent schistosome parasites in western Kenya. Mol. Ecol. 17 (2008) 5062-5074
59. Steinauer M.L., Mwangi I.N., Maina G.M., Kinuthia J.M., Mutuku M.W., Agola L.E., Mungai B.N., Mkoji G.M., and Loker E.S. Interactions between natural populations of human and rodent schistosomes in the Lake Victoria region of Kenya: a molecular epidemiological approach. PLos Neg. Trop. Dis. 2 (2008) 1-11
60. Steinmann P., Keiser J., Bos R., Tanner M., and Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis. 6 (2006) 411-425
61. Thiele E.A., Sorensen R.E., Gazzinelli A., and Minchella D.J. Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. Int. J. Parasitol. 38 (2008) 389-399
62. Tibayrenc M. Toward an integrated genetic epidemiology of parasitic protozoa and other pathogens. Annu. Rev. Genet. 33 (1999) 449-477
63. Truett G.E., Heeger P., Mynatt R.L., Truett A.A., Walker J.A., and Warman M.L. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). BioTechniques 29 (2000) 52-53
64. Van Oosterhout C., Hutchinson W.F., Wills D.P.M., and Shipley P. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 4 (2004) 535-538
65. Vekemans X., and Hardy O.J. New insights from fine-scale spatial genetic structure analyses in plant populations. Mol. Ecol. 13 (2004) 921-935
66. Vickery W.L., and Poulin R. Can helminth community patterns be amplified when transferred by predation from intermediate to definitive hosts?. J. Parasitol. 88 (2002) 650-656
67. Waghorn T.S., Leathwick D.M., Miller C.M., and Atkinson D.S. Brave or gullible: testing the concept that leaving susceptible parasites in refugia will slow the development of anthelmintic resistance. New Zealand Veterinary Journal 56 (2008) 158-163
68. Wang J.L. An estimator for pairwise relatedness using molecular markers. Genetics 160 (2002) 1203-1215
69. Waples R.S. Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. Journal of Heredity 89 (1998) 438-450
70. Weir B.S., and Cockerham C.C. Estimating F-statistics for the analysis of population structure. Evolution 38 (1984) 1358-1370
71. William S., Sabra A., Ramzy F., Mousa M., Demerdash Z., Bennett J.L., Day T.A., and Botros S. Stability and reproductive fitness of Schistosoma mansoni isolates with decreased sensitivity to praziquantel. Int. J. Parasitol. 31 (2001) 1093-1100
72. Wright S. The roles of mutation, inbreeding, crossbreeding and selection in evolution. Proceedings of the VI International Congress of Genetics 1 (1932) 356-366