Geographical genetic structure of Schistosoma japonicum revealed by analysis of mitochondrial DNA and microsatellite markers

Particle and Fibre Toxicology

Wei Hu³  Zheng Feng³  Bin Xu³  Zhong Yang⁴  Jing Su⁴  David Blair²  Donald P McManus¹  Hongyan Li⁴  Mingbo Yin³ 

[1] QIMR Berghofer Medical Research Institute, 300 Herston Road, Brisbane Qld 4029, Australia;School of Marine and Tropical Biology, James Cook University, Townsville Qld 4811, Australia;National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, 207 Rui Jin Er Road, Shanghai 200025, China;School of Life Science, Fudan University, Handan Road 220, Shanghai 200433, China

关键词: Microsatellite;    Mitochondrial DNA;    Population differentiation;    Genetic structure;    Genetic diversity;    Schistosoma japonicum;   

Others  :  1146658
DOI  :  10.1186/s13071-015-0757-x

 received in 2014-12-25, accepted in 2015-02-20,  发布年份 2015

【 摘 要 】

Background

Schistosoma japonicum is a significant public health risk in parts of China and elsewhere in Southeast Asia. To gain an insight into the epidemiology of schistosomiasis japonica, a detailed investigation of S. japonicum genetic population structure is needed.

Methods

Using three mitochondrial DNA fragments and ten microsatellite loci, we investigated the genetic diversity within and structure among twelve populations of S. japonicum sampled on a geographical scale covering most major endemic areas.

Results

Schistosoma japonicum lineages from Indonesia, the Philippines and Chinese Taiwan were clearly distinct from each other and from those in mainland China. Within mainland China, there was some evidence for genetic divergence between populations from the mountain and lake regions. However, the analysis inferred no clear sub-population structure in the lake region of mainland China. High genetic diversity was found among S. japonicum populations of mainland China and this was significantly higher than those from island regions.

Conclusions

High genetic diversity within and substantial differentiation among populations were demonstrated in S. japonicum.

【 授权许可】

   
2015 Yin et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis. 2006; 6(7):411-425.
• [2]King CH, Dickman K, Tisch DJ. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet. 2005; 365(9470):1561-1569.
• [3]Zhao QP, Sen Jiang M, Dong HF, Nie P. Diversification of Schistosoma japonicum in Mainland China Revealed by Mitochondrial DNA. Plos Neglect Trop D. 2012; 6(2):e1503.
• [4]Zhou XN, Guo JG, Wu XH, Jiang QW, Zheng J, Dang H et al.. Epidemiology of schistosomiasis in the People’s Republic of China, 2004. Emerg Infect Dis. 2007; 13(10):1470-1476.
• [5]Zhou XN, Bergquist R, Leonardo L, Yang GJ, Yang K, Sudomo M et al.. Schistosomiasis Japonica: Control and Research Needs. In: Advances in Parasitology, Vol 72: Important Helminth Infections in Southeast Asia: Diversity and Potential for Control and Elimination, Pt A. 2010.145-178.
• [6]Hope M, Foley DH, McManus DP. Electrophoretically detected allozyme variation reveals only moderate differentiation between Chinese and Philippine Schistosoma japonicum. Acta Trop. 1995; 60(2):101-108.
• [7]Bowles J, Hope M, Tiu WU, Liu XS, McManus DP. Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Trop. 1993; 55(4):217-229.
• [8]Sorensen E, Drew AC, Brindley PJ, Bogh HO, Gasser RB, Qian BZ et al.. Variation in the sequence of a mitochondrial NADH dehydrogenase I gene fragment among six natural populations of Schistosoma japonicum from China. Int J Parasitol. 1998; 28(12):1931-1934.
• [9]Gasser RB, Qian BZ, Nansen P, Johansen MV, Bogh H. Use of RAPD for the detection of genetic variation in the human blood fluke, Schistosoma japonicum, from mainland China. Mol Cell Probes. 1996; 10(5):353-358.
• [10]Shrivastava J, Qian BZ, McVean G, Webster JP. An insight into the genetic variation of Schistosoma japonicum in mainland China using DNA microsatellite markers. Mol Ecol. 2005; 14(3):839-849.
• [11]Zhao GH, Mo XH, Zou FC, Li J, Weng YB, Lin RQ et al.. Genetic variability among Schistosoma japonicum isolates from different endemic regions in China revealed by sequences of three mitochondrial DNA genes. Vet Parasitol. 2009; 162(1–2):67-74.
• [12]Rudge JW, Carabin H, Balolong E, Tallo V, Shrivastava J, Lu DB, Basanez M-G, Olveda R, McGarvey ST, Webster JP. Population Genetics of Schistosoma japonicum within the Philippines Suggest High Levels of Transmission between Humans and Dogs. Plos Neglect Trop D. 2008; 2(11):e340.
• [13]Woodruff DS, Merenlender AM, Upatham ES, Viyanant V. Genetic variation and differentiation of three Schistosoma species from the Philippines, Laos and Peninsular Malaysia. Am J Trop Med Hyg. 1987; 36(2):345-354.
• [14]Avise J. Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA; 2000.
• [15]Avise J. Molecular markers, natural history and evolution. 2nd ed. Sinuate, Sunderland, MA; 2004.
• [16]Allendorf FW, Seeb LW. Concordance of genetic divergence among sockeye salmon populations at allozyme, nuclear DNA, and mitochondrial DNA markers. Evolution. 2000; 54(2):640-651.
• [17]Lu G, Basley DJ, Bernatchez L. Contrasting patterns of mitochondrial DNA and microsatellite introgressive hybridization between lineages of lake whitefish (Coregonus clupeaformis); relevance for speciation. Mol Ecol. 2001; 10(4):965-985.
• [18]Ventura M, Petrusek A, Miro A, Hamrova E, Bunay D, De Meester L et al.. Local and regional founder effects in lake zooplankton persist after thousands of years despite high dispersal potential. Mol Ecol. 2014; 23(5):1014-1027.
• [19]Cummings MP, Otto SP, Wakeley J. Sampling properties of DNA sequence data in phylogenetic analysis. Mol Biol Evol. 1995; 12(5):814-822.
• [20]Rieseberg LH. Molecular ecology of hybridization. Advances in molecular ecology. Ios Press, Amsterdam; 1998.
• [21]Yin MB, Hu W, Mo XJ, Wang SY, Brindley PJ, McManus DP et al.. Multiple near-identical genotypes of Schistosoma japonicum can occur in snails and have implications for population-genetic analyses. Int J Parasitol. 2008; 38(14):1681-1691.
• [22]Excoffier L, Laval G, Schneider S. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol Bioinform. 2005; 1:47-50.
• [23]Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol. 2007; 24(8):1596-1599.
• [24]Bandelt HJ, Forster P, Rohl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999; 16(1):37-48.
• [25]Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009; 25(11):1451-1452.
• [26]Rousset F. GENEPOP ‘ 007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour. 2008; 8(1):103-106.
• [27]Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000; 155(2):945-959.
• [28]Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005; 14(8):2611-2620.
• [29]Fan P-C. The history of schistosomiasis japonica in Taiwan. Kaohsiung J Med Sci. 2006; 22(7):309-320.
• [30]Anou N, Yanwen X, Youren F. Schistosoma japonicum strains: Differentiation by RAPD and SSR-PCR. Southeast Asian J Trop Med Public Health. 2002; 33(4):720-724.
• [31]Zhao QP, Sen Jiang M, Littlewood DTJ, Nie P. Distinct Genetic Diversity of Oncomelania hupensis, Intermediate Host of Schistosoma japonicum in Mainland China as Revealed by ITS Sequences. Plos Neglect Trop D. 2010; 4(3):e611.
• [32]Liu Y, Lou T, Wang Y, Zhang W. Subspecies difference of oncomelaniid snails. Acta Zootaxonm Sin. 1981; 6:253-267.
• [33]Zhou XN. Population genetics morphology and distribution of Oncomelania hupensis, intermediate host of Schistosoma japonicum in mainland China. University of Copenhagen, Copenhagen; 1994.
• [34]Saijuntha W, Jarilla B, Leonardo A, Sunico L, Leonardo L, Andrews R et al.. Genetic Structure Inferred from Mitochondrial 12S Ribosomal RNA Sequence of Oncomelania quadrasi, the Intermediate Snail Host of Schistosoma japonicum in the Philippines. Am J Trop Med Hyg. 2014; 90(6):1140-1145.
• [35]Seto E, Xu B, Liang S, Gong P, Wu WP, Davis G et al.. The use of remote sensing for predictive modeling of schistosomiasis in China. Photogramm Eng Remote Sensing. 2002; 68(2):167-174.
• [36]Rudge JW, Lu DB, Fang GR, Wang TP, Basanez MG, Webster JP. Parasite genetic differentiation by habitat type and host species: molecular epidemiology of Schistosoma japonicum in hilly and marshland areas of Anhui Province. China Mol Ecol. 2009; 18(10):2134-2147.
• [37]Thiele EA, Sorensen RE, Gazzinelli A, Minchella DJ. Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. Int J Parasitol. 2008; 38(3–4):389-399.