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Molecular evolutionary analysis reveals Arctic-like rabies viruses evolved and dispersed independently in North and South Asia

  • Yu, Xin (School of Life Sciences, Ludong University) ;
  • Zhu, Hongwei (School of Life Sciences, Ludong University) ;
  • Bo, Yongheng (Shandong Provincial Key Laboratory of Quality Safety Monitoring and Risk Assessment for Animal Products) ;
  • Li, Youzhi (Shandong Provincial Key Laboratory of Quality Safety Monitoring and Risk Assessment for Animal Products) ;
  • Zhang, Jianlong (School of Life Sciences, Ludong University) ;
  • Jiang, Linlin (School of Life Sciences, Ludong University) ;
  • Chen, Guozhong (School of Life Sciences, Ludong University) ;
  • Zhang, Xingxiao (School of Life Sciences, Ludong University) ;
  • Wen, Yongjun (College of Veterinary Medicine, Inner Mongolia Agricultural University)
  • Received : 2020.07.10
  • Accepted : 2020.10.28
  • Published : 2021.01.31

Abstract

Background: Arctic-like (AL) lineages of rabies viruses (RABVs) remains endemic in some Arctic and Asia countries. However, their evolutionary dynamics are largely unappreciated. Objectives: We attempted to estimate the evolutionary history, geographic origin and spread of the Arctic-related RABVs. Methods: Full length or partial sequences of the N and G genes were used to infer the evolutionary aspects of AL RABVs by Bayesian evolutionary analysis. Results: The most recent common ancestor (tMRCA) of the current Arctic and AL RABVs emerged in the 1830s and evolved independently after diversification. Population demographic analysis indicated that the viruses experienced gradual growth followed by a sudden decrease in its population size from the mid-1980s to approximately 2000. Genetic flow patterns among the regions reveal a high geographic correlation in AL RABVs transmission. Discrete phylogeography suggests that the geographic origin of the AL RABVs was in east Russia in approximately the 1830s. The ancestral AL RABV then diversified and immigrated to the countries in Northeast Asia, while the viruses in South Asia were dispersed to the neighboring regions from India. The N and G genes of RABVs in both clades sustained high levels of purifying selection, and the positive selection sites were mainly found on the C-terminus of the G gene. Conclusions: The current AL RABVs circulating in South and North Asia evolved and dispersed independently.

Keywords

Acknowledgement

This work was supported by the National Key Research and Development Program of China (2016YFD0501001) and a grant from the Science and Technology Bureau of Yantai City, China (2019XDHZ094).

References

  1. King AM. Family-Rhabdoviridae, In: Adams MJ, Carstens EB, Lefkowitz EJ, editors. Virus Taxonomy. 1st ed. San Diego :Elsevier; 2012, 686-713.
  2. Bourhy H, Dautry-Varsat A, Hotez PJ, Salomon J. Rabies, still neglected after 125 years of vaccination. PLoS Negl Trop Dis. 2010;4(11):e839. https://doi.org/10.1371/journal.pntd.0000839
  3. Nadin-Davis SA, Real LA. Molecular phylogenetics of the lyssaviruses-insights from a coalescent approach. Adv Virus Res. 2011;79:203-238. https://doi.org/10.1016/B978-0-12-387040-7.00011-1
  4. Kuzmin IV, Hughes GJ, Botvinkin AD, Gribencha SG, Rupprecht CE. Arctic and Arctic-like rabies viruses: distribution, phylogeny and evolutionary history. Epidemiol Infect. 2008;136(4):509-519. https://doi.org/10.1017/S095026880700903X
  5. Nadin-Davis SA, Sheen M, Wandeler AI. Recent emergence of the Arctic rabies virus lineage. Virus Res. 2012;163(1):352-362. https://doi.org/10.1016/j.virusres.2011.10.026
  6. Pant GR, Lavenir R, Wong FY, Certoma A, Larrous F, Bhatta DR, et al. Recent emergence and spread of an Arctic-related phylogenetic lineage of rabies virus in Nepal. PLoS Negl Trop Dis. 2013;7(11):e2560. https://doi.org/10.1371/journal.pntd.0002560
  7. Kuzmin IV, Botvinkin AD, McElhinney LM, Smith JS, Orciari LA, Hughes GJ, et al. Molecular epidemiology of terrestrial rabies in the former Soviet Union. J Wildl Dis. 2004;40(4):617-631. https://doi.org/10.7589/0090-3558-40.4.617
  8. Horton DL, McElhinney LM, Freuling CM, Marston DA, Banyard AC, Goharrriz H, et al. Complex epidemiology of a zoonotic disease in a culturally diverse region: phylogeography of rabies virus in the Middle East. PLoS Negl Trop Dis. 2015;9(3):e0003569. https://doi.org/10.1371/journal.pntd.0003569
  9. Real LA, Russell C, Waller L, Smith D, Childs J. Spatial dynamics and molecular ecology of North American rabies. J Hered. 2005;96(3):253-260. https://doi.org/10.1093/jhered/esi031
  10. Bourhy H, Reynes JM, Dunham EJ, Dacheux L, Larrous F, Huong VT, et al. The origin and phylogeography of dog rabies virus. J Gen Virol. 2008;89(Pt 11):2673-2681. https://doi.org/10.1099/vir.0.2008/003913-0
  11. Nadin-Davis SA, Turner G, Paul JP, Madhusudana SN, Wandeler AI. Emergence of Arctic-like rabies lineage in India. Emerg Infect Dis. 2007;13(1):111-116. https://doi.org/10.3201/eid1301.060702
  12. Assenberg R, Delmas O, Morin B, Graham SC, De Lamballerie X, Laubert C, et al. Genomics and structure/function studies of Rhabdoviridae proteins involved in replication and transcription. Antiviral Res. 2010;87(2):149-161. https://doi.org/10.1016/j.antiviral.2010.02.322
  13. Jamil KM, Ahmed K, Hossain M, Matsumoto T, Ali MA, Hossain S, et al. Arctic-like rabies virus, Bangladesh. Emerg Infect Dis. 2012;18(12):2021-2024. https://doi.org/10.3201/eid1812.120061
  14. Shao XQ, Yan XJ, Luo GL, Zhang HL, Chai XL, Wang FX, et al. Genetic evidence for domestic raccoon dog rabies caused by Arctic-like rabies virus in Inner Mongolia, China. Epidemiol Infect. 2011;139(4):629-635. https://doi.org/10.1017/S0950268810001263
  15. Oem JK, Kim SH, Kim YH, Lee MH, Lee KK. Reemergence of rabies in the southern Han river region, Korea. J Wildl Dis. 2014;50(3):681-688. https://doi.org/10.7589/2013-07-177
  16. Oem JK, Kim SH, Kim YH, Lee MH, Lee KK. Complete genome sequences of three rabies viruses isolated from rabid raccoon dogs and a cow in Korea. Virus Genes. 2013;47(3):563-568. https://doi.org/10.1007/s11262-013-0923-1
  17. Oh SY, Kim SA, Kim JY, Yoo HS, Lee KK, Shin NS. Detection of antibodies against the rabies virus in Korean raccoon dogs (Nyctereutes procyonoides koreensis). J Zoo Wildl Med. 2012;43(1):174-176. https://doi.org/10.1638/2011-0063.1
  18. Tao XY, Guo ZY, Li H, Jiao WT, Shen XX, Zhu WY, et al. Rabies cases in the west of China have two distinct origins. PLoS Negl Trop Dis. 2015;9(10):e0004140. https://doi.org/10.1371/journal.pntd.0004140
  19. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969-1973. https://doi.org/10.1093/molbev/mss075
  20. Pond SL, Frost SD, Muse SV. HyPhy: hypothesis testing using phylogenies. Bioinformatics. 2005;21(5):676-679. https://doi.org/10.1093/bioinformatics/bti079
  21. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 2012;8(7):e1002764. https://doi.org/10.1371/journal.pgen.1002764
  22. Parker J, Rambaut A, Pybus OG. Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect Genet Evol. 2008;8(3):239-246. https://doi.org/10.1016/j.meegid.2007.08.001
  23. Lemey P, Rambaut A, Drummond AJ, Suchard MA. Bayesian phylogeography finds its roots. PLOS Comput Biol. 2009;5(9):e1000520. https://doi.org/10.1371/journal.pcbi.1000520
  24. Bielejec F, Rambaut A, Suchard MA, Lemey P. SPREAD: spatial phylogenetic reconstruction of evolutionary dynamics. Bioinformatics. 2011;27(20):2910-2912. https://doi.org/10.1093/bioinformatics/btr481
  25. Arai YT. [Phylogenetic analysis of two rabies viruses, Takamen and Komatsugawa strains isolated in Japan in the 1940's]. Kansenshogaku Zasshi. 2004;78(9):815-822. https://doi.org/10.11150/kansenshogakuzasshi1970.78.815
  26. Hyun BH, Lee KK, Kim IJ, Lee KW, Park HJ, Lee OS, et al. Molecular epidemiology of rabies virus isolates from South Korea. Virus Res. 2005;114(1-2):113-125. https://doi.org/10.1016/j.virusres.2005.06.004
  27. Tenzin WS, Wacharapluesadee S, Denduangboripant J, Dhand NK, Dorji R, Tshering D, et al. Rabies virus strains circulating in Bhutan: implications for control. Epidemiol Infect. 2011;139(10):1457-1462. https://doi.org/10.1017/S0950268810002682
  28. Tenzin SB, Sharma B, Dhand NK, Timsina N, Ward MP. Reemergence of rabies in Chhukha district, Bhutan, 2008. Emerg Infect Dis. 2010;16(12):1925-1930. https://doi.org/10.3201/eid1612.100958
  29. Ho SY, Shapiro B. Skyline-plot methods for estimating demographic history from nucleotide sequences. Mol Ecol Resour. 2011;11(3):423-434. https://doi.org/10.1111/j.1755-0998.2011.02988.x
  30. Sironi M, Cagliani R, Forni D, Clerici M. Evolutionary insights into host-pathogen interactions from mammalian sequence data. Nat Rev Genet. 2015;16(4):224-236. https://doi.org/10.1038/nrg3905
  31. Menezes R. Rabies in India. CMAJ. 2008;178(5):564-566. https://doi.org/10.1503/cmaj.071488
  32. Tao XY, Tang Q, Rayner S, Guo ZY, Li H, Lang SL, et al. Molecular phylodynamic analysis indicates lineage displacement occurred in Chinese rabies epidemics between 1949 to 2010. PLoS Negl Trop Dis. 2013;7(7):e2294. https://doi.org/10.1371/journal.pntd.0002294
  33. Zhu H, Chen X, Shao X, Ba H, Wang F, Wang H, et al. Characterization of a virulent dog-originated rabies virus affecting more than twenty fallow deer (Dama dama) in Inner Mongolia, China. Infect Genet Evol. 2015;31(4):127-134. https://doi.org/10.1016/j.meegid.2014.12.024
  34. Yang DK, Shin EK, Oh YI, Kang HK, Lee KW, Cho SD, et al. Molecular epidemiology of rabies virus circulating in South Korea, 1998-2010. J Vet Med Sci. 2011;73(8):1077-1082. https://doi.org/10.1292/jvms.10-0440