Stirred, not shaken: Genetic structure of the intermediate snail host Oncomelania hupensis robertsoni in an historically endemic schistosomiasis area

Parasites and Vectors

Volumn 4, Issue 1, 2011, Pages

  Hauswald, Anne Kathrin ^a   Remais, Justin V ^b,c   Xiao, Ning ^d   Davis, George M ^e   Lu, Ding ^d   Bale, Margaret J ^b   Wilke, Thomas ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b EMORY UNIVERSITY   (United States)

^c EMORY UNIVERSITY   (United States)

^d SICHUAN CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^e GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

AFLP; China; coevolution; cytochrome c oxidase subunit I (COI); Oncomelania hupensis robertsoni; phylogeny; phylogeography; schistosomiasis japonica; Sichuan Province; watersheds

Indexed keywords

CELL NUCLEUS DNA; MITOCHONDRIAL DNA; DNA;

ANIMAL EXPERIMENT; ARTICLE; CHINA; CONTROLLED STUDY; ENDEMIC DISEASE; GENETIC VARIABILITY; HOST; MANTEL HAENSZEL TEST; MOLECULAR CLOCK; MONOPHYLY; NONHUMAN; NUCLEOTIDE SEQUENCE; ONCOMELANIA HUPENSIS ROBERTSONI; PARASITE ISOLATION; PHYLOGENY; PHYLOGEOGRAPHY; POPULATION STRUCTURE; SCHISTOSOMA; SCHISTOSOMIASIS; SNAIL; SPACE; TAXONOMY; TIME; ANIMAL; BIOTA; CHEMISTRY; CLASSIFICATION; DNA SEQUENCE; GASTROPOD; GENETICS; GENOTYPE; MOLECULAR GENETICS;

ANIMALS; BIOTA; CHINA; DNA; GASTROPODA; GENOTYPE; MOLECULAR SEQUENCE DATA; PHYLOGEOGRAPHY; SEQUENCE ANALYSIS, DNA;

EID: 82455188247     PISSN: None     EISSN: 17563305     Source Type: Journal    
DOI: 10.1186/1756-3305-4-206     Document Type: Article

References (66)

1. The unacknowledged impact of chronic schistosomiasis. King CH, Dangerfield-Cha M, Chronic Illn 2008 4 65 79 10.1177/1742395307084407 18322031 (Pubitemid 351341878)
2. Transmission dynamics of Schistosoma japonicum in the lakes and marshlands of China. Gray DJ, Williams GM, Li Y, McManus DP, PLoS One 2008 3 4058 10.1371/journal.pone.0004058 19115007
3. A 5-year longitudinal study of schistosomiasis transmission in Shian village, the Anning River Valley, Sichuan Province, the Peoples' Republic of China. Zhu R, Gray DJ, Thrift AP, Williams GM, Zhang Y, Qiu D-C, Zheng F, Li Y-S, Guo J, Zhu H-Q, Wu W-P, Li RS, McManus DP, Parasites & Vectors 2011 4 43 10.1186/1756-3305-4-43 22033924
4. The public health significance and control of schistosomiasis in China-then and now. Zhou XN, Wang LY, Chen MG, Wu XH, Jiang QW, Chen XY, Zheng J, Utzinger J, Acta Trop 2005 96 97 105 10.1016/j.actatropica.2005.07.005 16125655 (Pubitemid 41463739)
5. Chapter 6-Schistosomiasis japonica: control and research needs. Zhou XN, Bergquist R, Leonardo L, Yang GJ, Yang K, Sudomo M, Olveda R, Adv Parasitol 2010 72 145 178 20624531
6. Genetic variation and differentiation of 3 Schistosoma species from the Philippines, Laos, and Peninsular Malaysia. Woodruff DS, Merenlender AM, Upatham ES, Viyanant V, Am J of Trop Med Hyg 1987 36 345 354 (Pubitemid 17057539)
7. Use of RAPD for the detection of genetic variation in the human blood fluke, Schistosoma japonicum, from mainland China. Gasser RB, Bao-Zhen Q, Nansen P, Johansen MV, Bøgh H, Mol Cell Probe 1996 10 353 358 10.1006/mcpr.1996.0048 (Pubitemid 26372355)
8. Tandemly repeated genomic sequence demonstrates inter- and intra-strain genetic variation in Schistosoma japonicum. Drew AC, Brindley PJ, Lewis FA, Liang YS, Minchella DJ, Trop Med Int Health 1998 3 373 380 10.1046/j.1365-3156. 1998.00228.x 9623942 (Pubitemid 28232298)
9. Variation in the sequence of a mitochondrial NADH dehydrogenase I gene fragment among six natural populations of Schistosoma japonicum from China. Sørensen E, Drew AC, Brindley PJ, Bøgh HO, Gasser RB, Qian BZ, Chiping Q, McManus DP, Int J Parasitol 1998 28 1931 1934 10.1016/S0020-7519(98) 00161-1 9925274 (Pubitemid 29017728)
10. An electrophoretic comparison of Schistosoma japonicum (Trematoda) from different provinces in the People's Republic of China suggests the existence of cryptic species. Chilton NB, Bao-Zhen Q, Bøgh HO, Nansen P, Parasitology 1999 119 375 383 10.1017/S0031182099004837 10581616 (Pubitemid 29479081)
11. Population genetics of multi-host parasites-the case for molecular epidemiological studies of Schistosoma japonicum using larval stages from naturally infected hosts. Shrivastava J, Gower CM, Balolong E, Wang TP, Qian BZ, Webster JP, Parasitology 2005 131 617 26 10.1017/S0031182005008413 16255820 (Pubitemid 41577935)
12. An insight into the genetic variation of Schistosoma japonicum in mainland China using DNA microsatellite markers. Shrivastava J, Qian BZ, Mcvean G, Webster JP, Mol Ecol 2005 14 839 49 10.1111/j.1365-294X.2005.02443.x 15723675 (Pubitemid 40346475)
13. Does multiple hosts mean multiple parasites? Population genetic structure of Schistosoma japonicum between definitive host species. Wang TP, Shrivastava J, Johansen MV, Zhang SQ, Wang FF, Webster JP, Int J Parasitol 2006 36 1317 1325 10.1016/j.ijpara.2006.06.011 16876170 (Pubitemid 44353487)
14. Multiple near-identical genotypes of Schistosoma japonicum can occur in snails and have implications for population-genetic analyses. Yin M, Hu W, Mo X, Wang S, Brindley PJ, McManus DP, Davis GM, Feng Z, Blair D, Int J Parasitol 2008 38 1681 1691 10.1016/j.ijpara.2008.05.015 18590733
15. New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. Liu F, Lu J, Hu W, Wang S-Y, Cui S-J, et al. PLoS Pathog 2006 2 4 29 10.1371/journal.ppat.0020029 16617374
16. Snail-Schistosoma, Paragonimus interaction in China: population ecology, genetic diversity, coevolution and emerging diseases. Davis GM, Wilke T, Zhang Y, Xu XJ, Qui PC, Spolsky CM, Qui DC, Li Y, Xia MY, Feng Z, Malacologia 1999 41 355 377 (Pubitemid 129321601)
17. Coevolution and compatibility in the snail-schistosome system. Webster JP, Davies CM, Parasitology 2001 126 41 56
18. Is host-schistosome coevolution going anywhere? Webster JP, Shrivastava J, Johnson PJ, Blair L, BMC Evol Biol 2007 7 91 10.1186/1471-2148-7-91 17567519 (Pubitemid 47078857)
19. Population genetics, micro-phylogeography, ecology, and susceptibility to schistosome infection of chinese Oncomelania hupensis hupensis (Gastropoda: Rissooidea: Pomatiopsidae) in the Miao river system. Shi CH, Wilke T, Davis GM, Xia MY, Qiu CP, Malacologia 2002 44 333 347 (Pubitemid 39260232)
20. Evolution of prosobranch snails transmitting Asian Schistosoma; coevolution with Schistosoma: a review. Davis GM, Prog Clin Parasitol 1992 3 145 204
21. Population genetics and systematic status of Oncomelania hupensis (Gastropoda: Pomatiopsidae) throughout China. Davis GM, Zhang Y, Guo YH, Spolsky CM, Malacologia 1995 37 133 156 (Pubitemid 126015028)
22. Cytochrome oxidase I-based phylogenetic relationships among the Pomatopsidae, Hydrobiidae, Rissoidae and Truncatellidae (Gastropoda: Caenogastropoda: Rissoacea). Davis GM, Wilke T, Spolsky C, Qiu CP, Qiu DC, Xia MY, Zhang Y, Rosenberg G, Malacologia 1998 40 251 266
23. Subspecific differentiation of oncomelaniid snails. Liu YY, Lou TK, Wang YX, Zhang WZ, Acta Zootaxonomica Sinica 1981 6 253 266
24. Genetic variability of Schistosoma japonicum (Katsorada, 1904) intermediate hosts Oncomelania hupensis (Gredler, 1881) (Gastropoda: Rissooidea). Zhou YB, Zhao GM, Jiang QW, Annal Zool (Wars) 2008 58 881 889
25. Landscape genetics: the correlation of spatial and genetic distances of Oncomelania hupensis, the intermediate host snail of Schistosoma japonicum in mainland China. Li SZ, Wang YX, Yang K, Liu Q, Wang Q, Zhang Y, Wu XH, Guo JG, Bergquist R, Zhou XN, Geospatial Health 2009 3 221 261 19440964
26. Extreme mitochondrial sequence diversity in the intermediate schistosomiasis host Oncomelania hupensis robertsoni: another case of ancestral polymorphism? Wilke T, Davis GM, Dongchuan Q, Spear RC, Malacologia 2006 48 143 157 (Pubitemid 44891284)
27. Distinct genetic diversity of Oncomelania hupensis, intermediate host of Schistosoma japonicum in Mainland China as revealed by ITS sequences. Zhao QP, Jiang MS, Littlewood DTJ, Nie P, PLoS Negl Trop Dis 2010 4 611 10.1371/journal.pntd.0000611 20209150
28. Molecular systematics of Hydrobiidae (Mollusca: Gastropoda: Rissooidea): testing monophyly and phylogenetic relationships. Wilke T, Davis GM, Falniowski A, Giusti F, Bodon M, Szarowska M, Proc Acad Nat Sci Philadelphia 2001 151 1 21 10.1635/0097-3157(2001)151[0001:MSOHMG]2.0.CO;2 (Pubitemid 33778738)
29. The phylogenetics of triculine snails (Rissooidea: Pomatiopsidae) from South-East Asia and Southern China: Historical biogeography and the transmission of human schistosomiasis. Attwood SW, Ambu S, Meng XH, Upatham ES, Xu FS, Southgate VR, J Mollus Stud 2003 69 263 271 10.1093/mollus/69.3.263 (Pubitemid 37089884)
30. The evolutionary genetics of speciation. Coyne JA, Orr HA, Philos T Roy Soc B 1998 353 287 305 10.1098/rstb.1998.0210 (Pubitemid 28153927)
31. Landscape pattern analysis and bayesian modelling for predicting Oncomelania hupensis distribution in Eryuan County, People' s Republic of China. Yang K, Zhou XN, Wu XH, Steinmann P, Wang XH, Am J Trop Med Hyg 2009 81 416 426 19706906
32. Effect of habitat fragmentation on the schistosome-transmitting snail Oncomelania hupensis in China. Zhou YB, Yang MX, Yihuo WL, Liu GM, Wang HY, Wei JG, Jiang QW, Trans R Soc Trop Med Hyg 2011 105 189 196 10.1016/j.trstmh.2010. 12.006 21367442
33. Erhaia (Gastropoda; Rissooidea): Phylogenetic relationships and the question of Paragonimus coevolution in Asia. Wilke T, Davis GM, Gong X, Liu HX, Am J Trop Med Hyg 2000 62 453 459 11220760 (Pubitemid 32164752)
34. Significance tests and weighted values for AFLP similarities, based on Arabidopsis in silico AFLP fragment length distributions. Koopman WJM, Gort G, Genetics 2004 167 1915 1928 10.1534/genetics.103.015693 15342529 (Pubitemid 39265927)
35. Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Vekemans X, Beauwens T, Lemaire M, Roldán-Ruiz I, Roldan-Ruiz I, Mol Ecol 2002 11 139 151 10.1046/j.0962-1083.2001.01415.x 11903911 (Pubitemid 34108478)
36. Homoplasy and distribution of AFLP fragments: an analysis in silico of the genome of different species. Caballero A, Quesada H, Mol Biol Evol 2010 27 5 1139 1151 10.1093/molbev/msq001 20056690
37. Differential gene expression in Schistosoma japonicum schistosomula from Wistar rats and BALB/c mice. Peng J, Han H, Gobert GN, Hong Y, Jiang W, Wang X, Fu Z, Liu J, Shi Y, Lin J, Parasites & Vectors 2011 4 155 10.1186/1756-3305-4-155 22033924
38. Schistosomiasis in the People's Republic of China: the era of the Three Gorges Dam. McManus DP, Gray DJ, Li Y, Feng Z, Williams GM, Stewart D, Rey-Ladino J, Ross AG, Clin Microbiol Rev 2010 26 442 466
39. Ecogenetics of shell sculpture in Oncomelania (Gastropoda) in canals of Hubei, China, and relevance for schistosome transmission. Davis GM, Wu WP, Xu XJ, Malacologia 2006 48 253 264 (Pubitemid 44891286)
40. Genetic traces of ancient demography. Harpending HC, Batzer MA, Gurven M, Jorde LB, Rogers AR, Sherry ST, Proc Natl Acad Sci USA 1998 95 1961 1967 10.1073/pnas.95.4.1961 9465125 (Pubitemid 28103502)
41. Snail hosts of Asian Schistosoma infecting man: evolution and coevolution. Davis GM, Malacol Rev Suppl 1980 2 195 268
42. Analytical methods for quantifying environmental connectivity for the control and surveillance of infectious disease spread. Remais J, Akullian A, Ding L, Seto E, J R Soc Interface 2010 7 1181 1193 10.1098/rsif.2009.0523 20164085
43. Hypsometric (area-altitude) analysis of erosional topology. Strahler AN, Geol Soc of Am Bull 1952 63 1117 1142 10.1130/0016-7606(1952)63[1117:HAAOET]2.0. CO;2
44. Integration of remote sensing data and GIS for accurate mapping of flooded areas. Brivio PA, Colombo R, Maggi M, Tomasoni R, Int J of Remote Sens 2002 26 429 441 (Pubitemid 34119881)
45. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R, Mol Mar Biol Biotechnol 1994 3 294 299 7881515
46. Infraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissooidea: Gastropoda): Do their different life histories affect biogeographic patterns and gene flow? Wilke T, Davis GM, Biol J Linn Soc 2000 70 89 105 10.1111/j.1095-8312.2000.tb00202.x
47. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Hall TA, Nucleic Acids Symp Ser 1999 41 95 98
48. AFLP: a new technique for DNA fingerprinting. Vos P, Hogers R, Bleeker M, Reijans M, vd Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Friters A, Paleman J, Zabeau M, Nucleic Acids Res 1995 26 4407 4414
49. Comparing geographical genetic differentiation between candidate and noncandidate loci for adaptation strengthens support for parallel ecological divergence in the marine snail Littorina saxatilis. Galindo J, Morán P, Rolán-Alvarez E, Mol Ecol 1990 18 919 930
50. jModelTest: Phylogenetic model averaging. Posada D, Mol Biol Evol 2008 25 1253 1256 10.1093/molbev/msn083 18397919 (Pubitemid 351882013)
51. Bayesian phylogenetics and its influence on insect systematics. Ronquist F, Deans AR, Annu Rev Entomol 2010 55 189 206 10.1146/annurev.ento.54.110807. 090529 19961329
52. Bayes factors. Kass RE, Raftery E, J Am Stat Assoc 1995 90 773 795 10.2307/2291091
53. BEAST: Bayesian evolutionary analysis by sampling trees. Drummond AJ, Rambaut A, BMC Evol Biol 2007 7 1 8 10.1186/1471-2148-7-1 17214884 (Pubitemid 46169607)
54. As time goes by: a simple fool's guide to molecular clock approaches in invertebrates. Wilke T, Schulthei R, Albrecht C, Am Malacol Bull 2009 27 25 45 10.4003/006.027.0203
55. TCS: a computer program to estimate gene genealogies. Clement M, Posada D, Crandall K, Mol Ecol 2000 9 1657 1660 10.1046/j.1365-294x.2000.01020.x 11050560
56. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Excoffier L, Laval G, Schneider S, Evol Bioinform Online 2005 1 47 50
57. A simulated annealing approach to define the genetic structure of populations. Dupanloup I, Schneider S, Excoffier L, Mol Ecol 2002 11 2571 2581 10.1046/j.1365-294X.2002.01650.x 12453240 (Pubitemid 35436677)
58. Population growth makes waves in the distribution of pairwise genetic differences. Rogers AR, Harpending H, Mol Biol Evol 1992 9 552 569 1316531
59. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Schneider S, Excoffier L, Genetics 1999 152 1079 1089 10388826 (Pubitemid 29330907)
60. Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Excoffier L, Mol Ecol 2004 13 853 864 10.1046/j.1365-294X.2003.02004.x 15012760 (Pubitemid 38390591)
61. An exact test for population differentiation. Raymond M, Rousset F, Evolution 1995 49 1280 1283 10.2307/2410454 (Pubitemid 3025486)
62. The detection of disease clustering and a generalized regression approach. Mantel N, Cancer Res 1967 27 209 220 6018555
63. Tools for population genetic analyses (TFPGA) version 1.3: a Windows program for the analysis of allozyme and molecular population genetic data. Miller MP, Department of Biological Sciences, Northern Arizona University, Flagstaff 1997
64. Application of phylogenetic networks in evolutionary studies. Huson DH, Bryant D, Mol Biol Evol 2006 32 254 267 (Pubitemid 43100040)
65. Estimation of average heterozygosity and genetic distance from a small number of individuals. Nei M, Genetics 1978 89 583 590 17248844 (Pubitemid 8396073)
66. Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Peakall R, Smouse PE, Mol Ecol Notes 2006 6 288 295 10.1111/j.1471-8286.2005.01155.x (Pubitemid 43373825)