Skip to main content
NCBI home page
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2022 Nov 11;66(4):861–874. doi: 10.1007/s11427-022-2221-5

Global patterns of phylogenetic diversity and transmission of bat coronavirus

Zhilin Wang 1,2,#, Guangping Huang 1, Mingpan Huang 1,2,#, Qiang Dai 3, Yibo Hu 1,2, Jiang Zhou 4, Fuwen Wei 1,2,5,✉
PMCID: PMC9664035  PMID: 36378474

Abstract

Bats are reservoirs for multiple coronaviruses (CoVs). However, the phylogenetic diversity and transmission of global bat-borne CoVs remain poorly understood. Here, we performed a Bayesian phylogeographic analysis based on 3,594 bat CoV RdRp gene sequences to study the phylogenetic diversity and transmission of bat-borne CoVs and the underlying driving factors. We found that host-switching events occurred more frequently for α-CoVs than for β-CoVs, and the latter was highly constrained by bat phylogeny. Bat species in the families Molossidae, Rhinolophidae, Miniopteridae, and Vespertilionidae had larger contributions to the cross-species transmission of bat CoVs. Regions of eastern and southern Africa, southern South America, Western Europe, and Southeast Asia were more frequently involved in cross-region transmission events of bat CoVs than other regions. Phylogenetic and geographic distances were the most important factors limiting CoV transmission. Bat taxa and global geographic hotspots associated with bat CoV phylogenetic diversity were identified, and bat species richness, mean annual temperature, global agricultural cropland, and human population density were strongly correlated with the phylogenetic diversity of bat CoVs. These findings provide insight into bat CoV evolution and ecological transmission among bat taxa. The identified hotspots of bat CoV evolution and transmission will guide early warnings of bat-borne CoV zoonotic diseases.

Supporting Information

The supporting information is available online at 10.1007/s11427-022-2221-5. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.

Keywords: bat, coronavirus, ecological transmission, phylogenetic diversity, driving factors

Electronic Supplementary Material

11427_2022_2221_MOESM1_ESM.pdf (2.4MB, pdf)

Global patterns of phylogenetic diversity and transmission of bat coronavirus

11427_2022_2221_MOESM2_ESM.xlsx (363.2KB, xlsx)

Supplementary material, approximately 363 KB.

11427_2022_2221_MOESM3_ESM.docx (17KB, docx)

Supplementary material, approximately 16.9 KB.

Footnotes

Compliance and ethics

The author(s) declare that they have no conflict of interest.

Contributed equally to this work

References

  1. Albery GF, Becker DJ, Brierley L, Brook CE, Christofferson RC, Cohen LE, Dallas TA, Eskew EA, Fagre A, Farrell MJ, et al. The science of the host-virus network. Nat Microbiol. 2021;6:1483–1492. doi: 10.1038/s41564-021-00999-5. [DOI] [PubMed] [Google Scholar]
  2. Anthony SJ, Johnson CK, Greig DJ, Kramer S, Che X, Wells H, Hicks AL, Joly DO, Wolfe ND, Daszak P, et al. Global patterns in coronavirus diversity. Virus Evol. 2017;3:vex012. doi: 10.1093/ve/vex012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M, Breit N, Olival KJ, Daszak P. Global hotspots and correlates of emerging zoonotic diseases. Nat Commun. 2017;8:1124. doi: 10.1038/s41467-017-00923-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Beyer RM, Manica A, Mora C. Shifts in global bat diversity suggest a possible role of climate change in the emergence of SARS-CoV-1 and SARS-CoV-2. Sci Total Environ. 2021;767:145413. doi: 10.1016/j.scitotenv.2021.145413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bielejec F, Baele G, Vrancken B, Suchard MA, Rambaut A, Lemey P. SpreaD3: interactive visualization of spatiotemporal history and trait evolutionary processes. Mol Biol Evol. 2016;33:2167–2169. doi: 10.1093/molbev/msw082. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Breed AC, Field HE, Smith CS, Edmonston J, Meers J. Bats without borders: long-distance movements and implications for disease risk management. EcoHealth. 2010;7:204–212. doi: 10.1007/s10393-010-0332-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Carlson CJ, Albery GF, Merow C, Trisos CH, Zipfel CM, Eskew EA, Olival KJ, Ross N, Bansal S. Climate change increases cross-species viral transmission risk. Nature. 2022;607:555–562. doi: 10.1038/s41586-022-04788-w. [DOI] [PubMed] [Google Scholar]
  8. Chen L, Liu B, Yang J, Jin Q. DBatVir: the database of bat-associated viruses. Database. 2014;2014:bau021. doi: 10.1093/database/bau021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cui J, Han N, Streicker D, Li G, Tang X, Shi Z, Hu Z, Zhao G, Fontanet A, Guan Y, et al. Evolutionary relationships between bat coronaviruses and their hosts. Emerg Infect Dis. 2007;13:1526–1532. doi: 10.3201/eid1310.070448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cui J, Li F, Shi ZL. Origin and evolution of pathogenic coronaviruses. Nat Rev Microbiol. 2019;17:181–192. doi: 10.1038/s41579-018-0118-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29:1969–1973. doi: 10.1093/molbev/mss075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ge XY, Wang N, Zhang W, Hu B, Li B, Zhang YZ, Zhou JH, Luo CM, Yang XL, Wu LJ, et al. Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft. Virol Sin. 2016;31:31–40. doi: 10.1007/s12250-016-3713-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hassanin A, Khouider S, Gembu GC, M. Goodman S, Kadjo B, Nesi N, Pourrut X, Nakouné E, Bonillo C. The comparative phylogeography of fruit bats of the tribe Scotonycterini (Chiroptera, Pteropodidae) reveals cryptic species diversity related to African Pleistocene forest refugia. Comptes Rendus Biologies. 2015;338:197–211. doi: 10.1016/j.crvi.2014.12.003. [DOI] [PubMed] [Google Scholar]
  14. Islam MS, Sazzad HMS, Satter SM, Sultana S, Hossain MJ, Hasan M, Rahman M, Campbell S, Cannon DL, Ströher U, et al. Nipah virus transmission from bats to humans associated with drinking traditional liquor made from date Palm Sap, Bangladesh, 2011–2014. Emerg Infect Dis. 2016;22:664–670. doi: 10.3201/eid2204.151747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. Global trends in emerging infectious diseases. Nature. 2008;451:990–993. doi: 10.1038/nature06536. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. Picante: R tools for integrating phylogenies and ecology. Bioinformatics. 2010;26:1463–1464. doi: 10.1093/bioinformatics/btq166. [DOI] [PubMed] [Google Scholar]
  17. Latinne A, Hu B, Olival KJ, Zhu G, Zhang L, Li H, Chmura AA, Field HE, Zambrana-Torrelio C, Epstein JH, et al. Origin and cross-species transmission of bat coronaviruses in China. Nat Commun. 2020;11:4235. doi: 10.1038/s41467-020-17687-3. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted]
  18. Lemey P, Rambaut A, Bedford T, Faria N, Bielejec F, Baele G, Russell CA, Smith DJ, Pybus OG, Brockmann D, et al. Unifying viral genetics and human transportation data to predict the global transmission dynamics of human influenza H3N2. PLoS Pathog. 2014;10:e1003932. doi: 10.1371/journal.ppat.1003932. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Letko M, Seifert SN, Olival KJ, Plowright RK, Munster VJ. Bat-borne virus diversity, spillover and emergence. Nat Rev Microbiol. 2020;18:461–471. doi: 10.1038/s41579-020-0394-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Li T, Tang X, Wu C, Yao X, Wang Y, Lu X, Lu J. The use of SARS-CoV-2-related coronaviruses from bats and pangolins to polarize mutations in SARS-Cov-2. Sci China Life Sci. 2020;63:1608–1611. doi: 10.1007/s11427-020-1764-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, et al. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310:676–679. doi: 10.1126/science.1118391. [DOI] [PubMed] [Google Scholar]
  22. Luby SP, Rahman M, Hossain MJ, Blum LS, Husain MM, Gurley E, Khan R, Ahmed BN, Rahman S, Nahar N, et al. Foodborne transmission of Nipah virus, Bangladesh. Emerg Infect Dis. 2006;12:1888–1894. doi: 10.3201/eid1212.060732. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Luo J, Jiang T, Lu G, Wang L, Wang J, Feng J. Bat conservation in China: should protection of subterranean habitats be a priority. Oryx. 2013;47:526–531. doi: 10.1017/S0030605311001505. [DOI] [Google Scholar]
  24. Mao XG, Zhu GJ, Zhang S, Rossiter SJ. Pleistocene climatic cycling drives intra-specific diversification in the intermediate horseshoe bat (Rhinolophus affinis) in Southern China. Mol Ecol. 2010;19:2754–2769. doi: 10.1111/j.1365-294X.2010.04704.x. [DOI] [PubMed] [Google Scholar]
  25. Minin VN, Suchard MA. Counting labeled transitions in continuous-time Markov models of evolution. J Math Biol. 2008;56:391–412. doi: 10.1007/s00285-007-0120-8. [DOI] [PubMed] [Google Scholar]
  26. Mollentze N, Streicker DG. Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proc Natl Acad Sci USA. 2020;117:9423–9430. doi: 10.1073/pnas.1919176117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Newbold T. Future effects of climate and land-use change on terrestrial vertebrate community diversity under different scenarios. Proc R Soc B. 2018;285:20180792. doi: 10.1098/rspb.2018.0792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Plowright RK, Parrish CR, McCallum H, Hudson PJ, Ko AI, Graham AL, Lloyd-Smith JO. Pathways to zoonotic spillover. Nat Rev Microbiol. 2017;15:502–510. doi: 10.1038/nrmicro.2017.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systatic Biol. 2018;67:901–904. doi: 10.1093/sysbio/syy032. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen) Virus Evol. 2016;2:vew007. doi: 10.1093/ve/vew007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rousset F, Ferdy JB. Testing environmental and genetic effects in the presence of spatial autocorrelation. Ecography. 2014;37:781–790. doi: 10.1111/ecog.00566. [DOI] [Google Scholar]
  32. Salah Uddin Khan M, Hossain J, Gurley ES, Nahar N, Sultana R, Luby SP. Use of infrared camera to understand bats’ access to date palm sap: implications for preventing Nipah virus transmission. EcoHealth. 2010;7:517–525. doi: 10.1007/s10393-010-0366-2. [DOI] [PubMed] [Google Scholar]
  33. Stoffberg S, Jacobs DS, Mackie IJ, Matthee CA. Molecular phylogenetics and historical biogeography of Rhinolophus bats. Mol Phylogenet Evol. 2010;54:1–9. doi: 10.1016/j.ympev.2009.09.021. [DOI] [PubMed] [Google Scholar]
  34. Streicker DG, Lemey P, Velasco-Villa A, Rupprecht CE. Rates of viral evolution are linked to host geography in bat rabies. PLoS Pathog. 2012;8:e1002720. doi: 10.1371/journal.ppat.1002720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, Rupprecht CE. Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science. 2010;329:676–679. doi: 10.1126/science.1188836. [DOI] [PubMed] [Google Scholar]
  36. Temmam S, Vongphayloth K, Baquero E, Munier S, Bonomi M, Regnault B, Douangboubpha B, Karami Y, Chrétien D, Sanamxay D, et al. Bat coronaviruses related to SARS-CoV-2 and infectious for human cells. Nature. 2022;604:330–336. doi: 10.1038/s41586-022-04532-4. [DOI] [PubMed] [Google Scholar]
  37. Watanabe S, Masangkay JS, Nagata N, Morikawa S, Mizutani T, Fukushi S, Alviola P, Omatsu T, Ueda N, Iha K, et al. Bat coronaviruses and experimental infection of bats, the Philippines. Emerg Infect Dis. 2010;16:1217–1223. doi: 10.3201/eid1608.100208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Webb CO, Ackerly DD, McPeek MA, Donoghue MJ. Phylogenies and community ecology. Annu Rev Ecol Syst. 2002;33:475–505. doi: 10.1146/annurev.ecolsys.33.010802.150448. [DOI] [Google Scholar]
  39. Willoughby A, Phelps K, Olival K. A comparative analysis of viral richness and viral sharing in cave-roosting bats. Diversity. 2017;9:35. doi: 10.3390/d9030035. [DOI] [Google Scholar]
  40. Wilson, D. E, Mittermeier, R. A. (2019). Handbook of the Mammals of the World. Vol. 9. Bats. Lynx Edicions, Barcelona.
  41. Xie W, Lewis PO, Fan Y, Kuo L, Chen MH. Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Systatic Biol. 2011;60:150–160. doi: 10.1093/sysbio/syq085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yang Q, Zhao X, Lemey P, Suchard MA, Bi Y, Shi W, Liu D, Qi W, Zhang G, Stenseth NC, et al. Assessing the role of live poultry trade in community-structured transmission of avian influenza in China. Proc Natl Acad Sci USA. 2020;117:5949–5954. doi: 10.1073/pnas.1906954117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Yin W, Mao C, Luan X, Shen DD, Shen Q, Su H, Wang X, Zhou F, Zhao W, Gao M, et al. Structural basis for inhibition of the RNA-dependent RNA polymerase from SARS-CoV-2 by remdesivir. Science. 2020;368:1499–1504. doi: 10.1126/science.abc1560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Zhou H, Ji J, Chen X, Bi Y, Li J, Wang Q, Hu T, Song H, Zhao R, Chen Y, et al. Identification of novel bat coronaviruses sheds light on the evolutionary origins of SARS-CoV-2 and related viruses. Cell. 2021;184:4380–4391. doi: 10.1016/j.cell.2021.06.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zhou P, Fan H, Lan T, Yang XL, Shi WF, Zhang W, Zhu Y, Zhang YW, Xie QM, Mani S, et al. Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature. 2018;556:255–258. doi: 10.1038/s41586-018-0010-9. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

11427_2022_2221_MOESM1_ESM.pdf (2.4MB, pdf)

Global patterns of phylogenetic diversity and transmission of bat coronavirus

11427_2022_2221_MOESM2_ESM.xlsx (363.2KB, xlsx)

Supplementary material, approximately 363 KB.

11427_2022_2221_MOESM3_ESM.docx (17KB, docx)

Supplementary material, approximately 16.9 KB.

Articles from Science China. Life Sciences are provided here courtesy of Nature Publishing Group

RESOURCES