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Genetic diversity and structure of Oncomelania hupensis hupensis in two eco-epidemiological settings as revealed by the mitochondrial COX1 gene sequences

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Abstract

Background

Oncomelania hupensis hupensis is the only intermediate host of Schistosoma japonicum, the causative agent of schistosomiasis in China and is therefore of significant medical and veterinary health importance. Although tremendous progress has been achieved, there remains an understudied area of approximately 2.06 billion m2 of potential snail habitats. This area could be further increased by annual flooding. Therefore, an understanding of population genetics of snails in these areas may be useful for future monitoring and control activities.

Methods and results

We sampled snails from Hexian (HX), Zongyang (ZY) and Shitai (ST) in Anhui (schistosomiasis transmission control), and from Hengtang (HT), Taicang (TC), Dongsan (DS) and Xisan (XS) in Jiangsu (schistosomiasis transmission interrupted), downstream of Anhui. ST, DS and XS are classified as hilly and mountainous areas, and HX, ZY, TC and HT as lake and marshland areas. The mitochondrial cytochrome c oxidase subunit I gene were sequenced. Out of 115 snails analyzed, 29 haplotypes were identified. We observed 56 (8.72%) polymorphic sites consisting of 51 transitions, four transversions and one multiple mutational change. The overall haplotype and nucleotide diversity were 0.899 and 0.01569, respectively. Snail populations in Anhui had higher genetic diversity than in Jiangsu. 73.32% of total variation was distributed among sites and 26.68% within sites. Snails were significantly separated according to eco-epidemiological settings in both network and phylogenetic analyses.

Conclusion

Our results could provide important guidance towards assessing coevolutionary interactions of snails with S. japonicum, as well as for future molluscan host monitoring and control activities.

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References

  1. Saijuntha W, Jarilla B, Leonardo AK, Sunico LS, Leonardo LR, Andrews RH et al (2014) 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 90(6):1140–1145. https://doi.org/10.4269/ajtmh.13-0260

    Article  PubMed  PubMed Central  Google Scholar 

  2. Chen J, Xu J, Bergquist R, Li SZ, Zhou XN (2018) “Farewell to the God of Plague”: the importance of political commitment towards the elimination of schistosomiasis. Trop Med Infect Dis. https://doi.org/10.3390/tropicalmed3040108

    Article  PubMed  PubMed Central  Google Scholar 

  3. Yang K, Wang XH, Yang GJ, Wu XH, Qi YL, Li HJ et al (2008) An integrated approach to identify distribution of Oncomelania hupensis, the intermediate host of Schistosoma japonicum, in a mountainous region in China. Int J Parasitol 38(8–9):1007–1016. https://doi.org/10.1016/j.ijpara.2007.12.007

    Article  PubMed  Google Scholar 

  4. Qian MB, Chen J, Bergquist R, Li ZJ, Li SZ, Xiao N et al (2019) Neglected tropical diseases in the People’s Republic of China: progress towards elimination. Infect Dis Poverty 8(1):86. https://doi.org/10.1186/s40249-019-0599-4

    Article  PubMed  PubMed Central  Google Scholar 

  5. Zhang LJ, Xu ZM, Yang F, Dang H, Li YL, Lu S et al (2021) Endemic status of schistosomiasis in People’ Republic of China in 2020. Chin J Schistosomiasis Control. https://doi.org/10.16250/j.32.1374.2021109

    Article  Google Scholar 

  6. McGarvey ST, Carabin H, Balolong E Jr, Belisle P, Fernandez T, Joseph L et al (2006) Cross-sectional associations between intensity of animal and human infection with Schistosoma japonicum in Western Samar province, Philippines. Bull World Health Organ 84(6):446–452. https://doi.org/10.2471/blt.05.026427

    Article  PubMed  PubMed Central  Google Scholar 

  7. Yang K, Yang GJ, Hong QB, Huang YX, Sun LP, Gao Y et al (2012) Surveillance of schistosomiasis in Jiangsu Province, China, 2005–2010. Chin J Schistosomiasis Control 24(05):527–532

    Google Scholar 

  8. Gao FH, Zhang SQ, Wang TP, He JC, Li TT, Xu XJ et al (2020) Spatiotemporal distribution of Oncomelania hupensis snail habitats in Anhui Province. Chin J Schistosomiasis Control 32(02):140–147

    CAS  Google Scholar 

  9. Lu DB, Wang TP, Rudge JW, Donnelly CA, Fang GR, Webster JP (2010) Contrasting reservoirs for Schistosoma japonicum between marshland and hilly regions in Anhui, China–a two-year longitudinal parasitological survey. Parasitology 137(1):99–110. https://doi.org/10.1017/S003118200999103X

    Article  PubMed  Google Scholar 

  10. Zou HY, Yu QF, Qiu C, Webster JP, Lu DB (2020) Meta-analyses of Schistosoma japonicum infections in wild rodents across China over time indicates a potential challenge to the 2030 elimination targets. PLoS Negl Trop Dis 14(9):e0008652. https://doi.org/10.1371/journal.pntd.0008652

    Article  PubMed  PubMed Central  Google Scholar 

  11. Li ZJ, Ge J, Dai JR, Wen LY, Lin DD, Madsen H et al (2016) Biology and control of snail intermediate host of Schistosoma japonicum in The People’s Republic of China. Adv Parasitol 92:197–236. https://doi.org/10.1016/bs.apar.2016.02.003

    Article  PubMed  Google Scholar 

  12. Ross AG, Sleigh AC, Li Y, Davis GM, Williams GM, Jiang Z et al (2001) Schistosomiasis in the People’s Republic of China: prospects and challenges for the 21st century. Clin Microbiol Rev 14(2):270–295. https://doi.org/10.1128/CMR.14.2.270-295.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Davis GM, Wilke T, Zhang Y, Xu XJ, Qui CP, Spolsky CM et al (1999) Snail-Schistosoma, Paragonimus interaction in China: population ecology, genetic diversity, coevolution and emerging diseases. Malacologia 41(2):355–377

    Google Scholar 

  14. Wilke T, Davis GM, Cui EC, Xiao-Nung Z, Xiao Peng Z, Yi Z et al (2000) Oncomelania hupensis (Gastropoda: rissooidea) in eastern China: molecular phylogeny, population structure, and ecology. Acta Trop 77(2):215–227

    Article  CAS  PubMed  Google Scholar 

  15. Shi CH, Wilke T, Davis GM, Xia MY, Qiu CP (2002) Population genetics, microphylogeography, ecology and susceptibility to schistosome infection of Chinese Oncomelania hupensis hupensis (Gastropoda: Rissooidea: Pomatiopsidae) in the Miao river system. Malacologia 44(2):333–347

    Google Scholar 

  16. Zhao QP, Jiang MS, Littlewood DT, Nie P (2010) Distinct genetic diversity of Oncomelania hupensis, intermediate host of Schistosoma japonicum in mainland China as revealed by ITS sequences. PLoS Negl Trop Dis 4(3):e611. https://doi.org/10.1371/journal.pntd.0000611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Li SZ, Wang YX, Yang K, Liu Q, Wang Q, Zhang Y et al (2009) Landscape genetics: the correlation of spatial and genetic distances of Oncomelania hupensis, the intermediate host snail of Schistosoma japonicum in mainland China. Geospat Health 3(2):221–231. https://doi.org/10.4081/gh.2009.222

    Article  PubMed  Google Scholar 

  18. Guan W, Li SZ, Abe EM, Webster BL, Rollinson D, Zhou XN (2016) The genetic diversity and geographical separation study of Oncomelania hupensis populations in mainland China using microsatellite loci. Parasites Vectors 9(1):28

    Article  PubMed  PubMed Central  Google Scholar 

  19. Wilke T, Davis GM (2000) Infraspecific mitochondrial sequence diversity in Hydrobia ulvae and Hydrobia ventrosa (Hydrobiidae: Rissooidea: Gastropoda): do their different life histories affect biogeographic patterns and gene flow? Biol J Lin Soc 70:89–105

    Article  Google Scholar 

  20. Brown WM, George M Jr, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76(4):1967–1971. https://doi.org/10.1073/pnas.76.4.1967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Mueller RL, Macey JR, Jaekel M, Wake DB, Boore JL (2004) Morphological homoplasy, life history evolution, and historical biogeography of plethodontid salamanders inferred from complete mitochondrial genomes. Proc Natl Acad Sci USA 101(38):13820–13825. https://doi.org/10.1073/pnas.0405785101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ohiolei JA, Luka J, Zhu GQ, Yan HB, Li L, Magaji AA et al (2019) First molecular description, phylogeny and genetic variation of Taenia hydatigena from Nigerian sheep and goats based on three mitochondrial genes. Parasites Vectors 12(1):520. https://doi.org/10.1186/s13071-019-3780-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Wei SJ, Tang P, Zheng LH, Shi M, Chen XX (2010) The complete mitochondrial genome of Evania appendigaster (Hymenoptera: Evaniidae) has low A+T content and a long intergenic spacer between atp8 and atp6. Mol Biol Rep 37(4):1931–1942. https://doi.org/10.1007/s11033-009-9640-1

    Article  CAS  PubMed  Google Scholar 

  24. Qiu C, Lu DB, Deng Y, Zou HY, Liang YS, Webster JP (2019) Population genetics of Oncomelania hupensis snails, intermediate hosts of Schistosoma japonium, from emerging, re-emerging or established habitats within China. Acta Trop 197:105048. https://doi.org/10.1016/j.actatropica.2019.105048

    Article  PubMed  Google Scholar 

  25. Ding H, Lu DB, Gao YM, Deng Y, Li Y (2017) Genetic diversity and structure of Schistosoma japonicum within two marshland villages of Anhui, China, prior to schistosome transmission control and elimination. Parasitol Res 116(2):569–576. https://doi.org/10.1007/s00436-016-5321-x

    Article  PubMed  Google Scholar 

  26. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25(24):4876–4882. https://doi.org/10.1093/nar/25.24.4876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rozas J, Ferrer-Mata A, Sanchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE et al (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34(12):3299–3302. https://doi.org/10.1093/molbev/msx248

    Article  CAS  PubMed  Google Scholar 

  28. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123(3):585–595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Excoffier L, Laval G, Schneider S (2007) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed  PubMed Central  Google Scholar 

  31. Felsenstein J (2005) PHYLIP (phylogeny inference package) version 3.6. Department of Genome Sciences, University of Washington, Seattle, WA

    Google Scholar 

  32. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Sun LP, Wang W, Hong QB, Li SZ, Liang YS, Yang HT et al (2017) Approaches being used in the national schistosomiasis elimination programme in China: a review. Infect Dis Poverty 6(1):55. https://doi.org/10.1186/s40249-017-0271-9

    Article  PubMed  PubMed Central  Google Scholar 

  34. Sun LP, Liang YS, Wu HH, Tian ZX, Dai JR, Yang K et al (2011) A Google Earth-based surveillance system for schistosomiasis japonica implemented in the lower reaches of the Yangtze River. China Parasites Vectors 4:223

    Article  PubMed  Google Scholar 

  35. Lei ZL, Zhou XN (2015) Eradication of schistosomiasis: a new target and a new task for the National Schistosomiasis Control Porgramme in the People’s Republic of China. Chin J Schistosomiasis Control 27(1):1–4

    Google Scholar 

  36. Wright S (1978) Evolution and genetics of populations. Volume 4. Variability within and among natural populations, vol 4. University of Chicago Press, Chicago

    Google Scholar 

  37. Hauswald AK, Remais JV, Xiao N, Davis GM, Lu D, Bale MJ et al (2011) Stirred, not shaken: genetic structure of the intermediate snail host Oncomelania hupensis robertsoni in an historically endemic schistosomiasis area. Parasites Vectors 4:206

    Article  PubMed  PubMed Central  Google Scholar 

  38. Lu DB, Yu QF, Zhang JY, Sun MT, Gu MM, Webster JP et al (2021) Extended survival and reproductive potential of single-sex male and female Schistosoma japonicum within definitive hosts. Int J Parasitol. https://doi.org/10.1016/j.ijpara.2021.03.005

    Article  PubMed  Google Scholar 

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Acknowledgements

We are very grateful to Prof. Joanne P. Webster from Royal Veterinary College, University of London for her great help in improving the quality of the English language in the article.

Funding

The authors are currently funded by the National Science Foundation of China (to DL, No. 81971957), by the Suzhou-2019′ 18th scientific and technological development projects (Minsheng Technology) (to ZZ, No. SS2019044).

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Author notes

  1. Jie-Ying Zhang and Man-Man Gu have contributed equally to this work and are co-first authors.

Authors and Affiliations

  1. Department of Epidemiology and Statistics, School of Public Health, Soochow University, Suzhou, China

    Jie-Ying Zhang, Man-Man Gu, Qiu-Fu Yu, Meng-Tao Sun, Hui-Ying Zou & Da-Bing Lu

  2. Center for Disease Prevention and Control of Wuzhong District, Suzhou, China

    Zhi-Jun Zhou

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Contributions

DL, JZ and MG contributed to the study conception and design. All authors performed the experiments. The first draft of the manuscript was written by JZ and MG, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Da-Bing Lu.

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This article does not contain any studies with human participants performed by any of the authors. All authors have given their consent to participate in this study and submit it to Molecular Biology Reports.

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11033_2021_6907_MOESM4_ESM.tiff

Supplementary Fig. S1 Phylogram of O. h. hupensis based on COX1 sequences. Values beside the branch represent posterior probabilities in which the node was recovered for NJ via 1000 bootstrap pseudo-replicates. The letters after each branch represent different haplotype individuals coded by Haplotype No. and its detailed sites. O. h. quadrasi was obtained from GenBank under accession No. LC276227.1 and was used as an out-group. (TIFF 2150 KB)

Supplementary Fig. S2 Phylogram of O. h. hupensis based on maximum likelihood (ML) analysis. (TIFF 895 KB)

Supplementary Fig. S3 Phylogram of O. h. hupensis based on minimum evolution (ME) analysis. (TIFF 1239 KB)

Supplementary Fig. S4 Phylogram of O. h. hupensis based on maximum parsimony (MP) analysis. (TIFF 387 KB)

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Zhang, JY., Gu, MM., Yu, QF. et al. Genetic diversity and structure of Oncomelania hupensis hupensis in two eco-epidemiological settings as revealed by the mitochondrial COX1 gene sequences. Mol Biol Rep 49, 511–518 (2022). https://doi.org/10.1007/s11033-021-06907-8

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