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Phylodynamic and transmission pattern of rabies virus in China and its neighboring countries

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Abstract

Rabies is a fatal disease caused by infection with rabies virus (RABV), and human rabies is still a critical public-health concern in China. Although there have been some phylogenetic studies about RABV transmission patterns, with the accumulation of more rabies sequences in recent years, there is an urgent need to update and clarify the spatial and temporal patterns of RABV circulating in China on a national scale. In this study, we collected all available RABV nucleoprotein gene sequences from China and its neighboring countries and performed comparative analysis. We identified six significant subclades of RABV circulating in China and found that each of them has a specific geographical distribution, reflecting possible physical barriers to gene flow. The phylogeographic analysis revealed minimal viral movement among different geographical locations. An analysis using Bayesian coalescent methods indicated that the current RABV strains in China may come from a common ancestor about 400 years ago, and currently, China is amid the second event of increasing RABV population since the 1950s, but the population has decreased gradually. We did not detect any evidence of recombination in the sequence dataset, nor did we find any evidence for positive selection during the expansion of RABV. Overall, geographic location and neutral genetic drift may be the main factors in shaping the phylogeography of RABV transmission in China.

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References

  1. Bourhy H, Reynes JM, Dunham EJ, Dacheux L, Larrous F, Huong VTO, Xu GL, Yan JX, Miranda MEG, Holmes EC (2008) The origin and phylogeography of dog rabies virus. J Gen Virol 89:2673–2681

    Article  CAS  PubMed  Google Scholar 

  2. Hampson K, Coudeville L, Lembo T, Sambo M, Kieffer A, Attlan M, Barrat J, Blanton JD, Briggs DJ, Cleaveland S, Costa P, Freuling CM, Hiby E, Knopf L, Leanes F, Meslin FX, Metlin A, Miranda ME, Muller T, Nel LH, Recuenco S, Rupprecht CE, Schumacher C, Taylor L, Vigilato MAN, Zinsstag J, Dushoff J, Par GARC (2015) Estimating the global burden of endemic canine rabies. Plos Neglect Trop Dis 9(4):3709

    Article  Google Scholar 

  3. Yin WW, Dong J, Tu CC, Edwards J, Guo FS, Zhou H, Yu HJ, Vong S, Board RTA (2013) Challenges and needs for China to eliminate rabies. Infect Dis Poverty 2:23

    Article  PubMed  PubMed Central  Google Scholar 

  4. Abbas SS, Kakkar M (2015) Rabies control in India: a need to close the gap between research and policy. B World Health Organ 93(2):131–132

    Article  Google Scholar 

  5. Knobel DL, Cleaveland S, Coleman PG, Fevre EM, Meltzer MI, Miranda MEG, Shaw A, Zinsstag J, Meslin FX (2005) Re-evaluating the burden of rabies in Africa and Asia. B World Health Organ 83(5):360–368

    Google Scholar 

  6. Troupin C, Dacheux L, Tanguy M, Sabeta C, Blanc H, Bouchier C, Vignuzzi M, Duchene S, Holmes EC, Bourhy H (2016) Large-scale phylogenomic analysis reveals the complex evolutionary history of rabies virus in multiple carnivore hosts. PLoS Pathog 12(12):e1006041

    Article  PubMed  PubMed Central  Google Scholar 

  7. Zhang Y, Vrancken B, Feng Y, Dellicour S, Yang Q, Yang W, Zhang Y, Dong L, Pybus OG, Zhang H, Tian H (2017) Cross-border spread, lineage displacement and evolutionary rate estimation of rabies virus in Yunnan Province, China. Virol J 14(1):102

    Article  PubMed  PubMed Central  Google Scholar 

  8. Zhang JM, Zhang ZS, Deng YQ, Wu SL, Wang W, Yan YS (2017) Incidence of human rabies and characterization of rabies virus nucleoprotein gene in dogs in Fujian Province, Southeast China, 2002–2012. BMC Infect Dis 17:599

    Article  PubMed  PubMed Central  Google Scholar 

  9. Liu Y, Zhang HP, Zhang SF, Wang JX, Zhou HN, Zhang F, Wang YM, Ma L, Li N, Hu RL (2016) Rabies outbreaks and vaccination in domestic camels and cattle in Northwest China. Plos Neglect Trop Dis 10(9):e0004890

    Article  Google Scholar 

  10. Feng Y, Shi YY, Yu MY, Xu WD, Gong WJ, Tu ZZ, Ding LX, He B, Guo HC, Tu CC (2016) Livestock rabies outbreaks in Shanxi province, China. Arch Virol 161(10):2851–2854

    Article  CAS  PubMed  Google Scholar 

  11. Yu JN, Li H, Tang Q, Rayner S, Han N, Guo ZY, Liu HZ, Adams J, Fang W, Tao XY, Wang SM, Liang GD (2012) The spatial and temporal dynamics of rabies in China. Plos Neglect Trop Dis 6(5):1640

    Article  Google Scholar 

  12. Yao HW, Yang Y, Liu K, Li XL, Zuo SQ, Sun RX, Fang LQ, Cao WC (2015) The spatiotemporal expansion of human rabies and its probable explanation in mainland China, 2004–2013. Plos Neglect Trop Dis 9(2):e0003502

    Article  Google Scholar 

  13. Guo ZY, Tao XY, Yin CP, Han N, Yu JN, Li H, Liu HZ, Fang W, Adams J, Wang J, Liang GD, Tang Q, Rayner S (2013) National borders effectively halt the spread of rabies: the current rabies epidemic in China is dislocated from cases in neighbouring countries. Plos Neglect Trop Dis 7(1):e2039

    Article  Google Scholar 

  14. Wang LH, Tang Q, Liang GD (2014) Rabies and rabies virus in wildlife in mainland China, 1990–2013. Int J Infect Dis 25:122–129

    Article  PubMed  Google Scholar 

  15. Meng SL, Sun Y, Wu XF, Tang JR, Xu GL, Lei YL, Wu J, Yan JX, Yang XM, Rupprecht CE (2011) Evolutionary dynamics of rabies viruses highlights the importance of China rabies transmission in Asia. Virology 410(2):403–409

    Article  CAS  PubMed  Google Scholar 

  16. Finke S, Conzelmann KK (2005) Replication strategies of rabies virus. Virus Res 111(2):120–131

    Article  CAS  PubMed  Google Scholar 

  17. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B (2015) RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1(1):vev003

    Article  PubMed  PubMed Central  Google Scholar 

  18. Li WZ, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22(13):1658–1659

    Article  CAS  PubMed  Google Scholar 

  19. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Rambaut A, Lam TT, Carvalho LM, Pybus OG (2016) Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2(1):vew007

    Article  PubMed  PubMed Central  Google Scholar 

  21. Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32(1):268–274

    Article  CAS  PubMed  Google Scholar 

  22. Xia XH (2017) DAMBE6: new tools for microbial genomics, phylogenetics, and molecular evolution. J Hered 108(4):431–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14(6):587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Minh BQ, Nguyen MAT, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30(5):1188–1195

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yu GC, Smith DK, Zhu HC, Guan Y, Lam TTY (2017) GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8(1):28–36

    Article  Google Scholar 

  26. Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4(1):vey016

    Article  PubMed  PubMed Central  Google Scholar 

  27. Baele G, Lemey P, Bedford T, Rambaut A, Suchard MA, Alekseyenko AV (2012) Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Mol Biol Evol 29(9):2157–2167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Baele G, Li WL, Drummond AJ, Suchard MA, Lemey P (2013) Accurate model selection of relaxed molecular clocks in bayesian phylogenetics. Mol Biol Evol 30(2):239–243

    Article  CAS  PubMed  Google Scholar 

  29. Bielejec F, Baele G, Vrancken B, Suchard MA, Rambaut A, Lemey P (2016) Sprea D3: interactive visualization of spatiotemporal history and trait evolutionary processes. Mol Biol Evol 33(8):2167–2169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3(5):418–426

    CAS  PubMed  Google Scholar 

  31. Weaver S, Shank SD, Spielman SJ, Li M, Muse SV, Pond SLK (2018) Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol Biol Evol 35(3):773–777

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. Pond SLK, Frost SDW (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22(5):1208–1222

    Article  CAS  Google Scholar 

  33. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Pond SLK (2012) Detecting individual sites subject to episodic diversifying selection. Plos Genet 8(7):e1002764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Pond SLK, Scheffler K (2013) FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 30(5):1196–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Tsai KJ, Hsu WC, Chuang WC, Chang JC, Tu YC, Tsai HJ, Liu HF, Wang FI, Lee SH (2016) Emergence of a sylvatic enzootic formosan ferret badger-associated rabies in Taiwan and the geographical separation of two phylogenetic groups of rabies viruses. Vet Microbiol 182:28–34

    Article  CAS  PubMed  Google Scholar 

  36. Zhou H, Vong S, Liu K, Li Y, Mu D, Wang LP, Yin WW, Yu HJ (2016) Human Rabies in China, 1960–2014: a descriptive epidemiological study. Plos Neglected Tropical Diseases 10(8):e0004874

    Article  PubMed  PubMed Central  Google Scholar 

  37. Perez-Losada M, Arenas M, Galan JC, Palero F, Gonzalez-Candelas F (2015) Recombination in viruses: mechanisms, methods of study, and evolutionary consequences. Infect Genet Evol 30:296–307

    Article  CAS  PubMed  Google Scholar 

  38. Baghi HB, Bazmani A, Aghazadeh M (2016) The fight against rabies: the Middle East needs to step up its game. Lancet 388(10054):1880

    Article  PubMed  Google Scholar 

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Correspondence to Jianqiang Du.

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Wang, L., Wu, X., Bao, J. et al. Phylodynamic and transmission pattern of rabies virus in China and its neighboring countries. Arch Virol 164, 2119–2129 (2019). https://doi.org/10.1007/s00705-019-04297-8

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  • DOI: https://doi.org/10.1007/s00705-019-04297-8

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