During the last few decades, bat lyssaviruses have become the topic of intensive molecular and epidemiological investigations. Since ancient times, rhabdoviruses have caused fatal encephalitis in humans which has led to research into effective strategies for their eradication. Modelling of potential future cross-species virus transmissions forms a substantial component of the recent infection biology of rabies. In this article, we summarise the available data on the phylogeography of both bats and lyssaviruses in Europe and the adjacent reg ions, especially in the contact zone between the Palearctic and Ethiopian realms. Within these zones, three bat families are present with high potential for cross-species transmission and the spread of lyssaviruses in Phylogroup II to Europe (part of the western Palearctic). The lack of effective therapies for rabies viruses in Phylogroup II and the most divergent lyssaviruses generates impetus for additional phylogenetic and virological research within this geographical region.

Department of Ecology and Diseases of Zoo Animals Game Fish and Bees University of Veterinary Sciences Brno Palackého tř 1946 1 612 42 Brno Czech Republic

Faculty of Biology University of Plovdiv Paisii Hilendarski 24 Tzar Assen Str 4000 Plovdiv Bulgaria

Institute of Biodiversity and Ecosystem Research Bulgarian Academy of Sciences 1 Tsar Osvoboditel Blvd 1000 Sofia Bulgaria

Institute of Vertebrate Biology Czech Academy of Sciences Květná 8 603 65 Brno Czech Republic

National Centre of Infectious and Parasitic Diseases 26 Yanko Sakazov Blvd 1504 Sofia Bulgaria

Zobrazit více v PubMed

Ruedi M., Stadelmann B., Gager Y., Douzery E.J., Francis C.M., Lin L.K., Guillén-Servent A., Cibois A. Molecular phylogenetic reconstructions identify East Asia as the cradle for the evolution of the cosmopolitan genus Myotis (Mammalia, Chiroptera) Mol. Phylogenet. Evol. 2013;69:437–449. doi: 10.1016/j.ympev.2013.08.011. PubMed DOI

Teeling E.C., Vernes S.C., Dávalos L.M., Ray D.A., Gilbert M.T.P., Myers E. Bat1K Consortium. Bat Biology, Genomes, and the Bat1K Project: To Generate Chromosome-Level Genomes for All Living Bat Species. Annu. Rev. Anim. Biosci. 2018;6:23–46. doi: 10.1146/annurev-animal-022516-022811. PubMed DOI

Teeling E.C., Jones G., Rossiter S.J. Bat Bioacoustics. Springer; New York, NY, USA: 2016. Phylogeny, genes, and hearing: Implications for the evolution of echolocation in bats; pp. 25–54.

Simmons N.B., Cirranello A.L. Bat Species of the World: A Taxonomic and Geographic Database, Version 1.3. 2023. 2023. [(accessed on 8 August 2023)]. Available online: https://batnames.org/

Wackermannová M., Pinc L., Jebavý L. Olfactory sensitivity in mammalian species. Physiol. Res. 2016;65:369. doi: 10.33549/physiolres.932955. PubMed DOI

Wilkinson G.S., Adams D.M., Haghani A., Lu A.T., Zoller J., Breeze C.E., Arnold B.D., Ball H.C., Carter G.G., Cooper L.N., et al. Genome Methylation Predicts Age and Longevity of Bats. Nat. Commun. 2021;12:1615. doi: 10.1038/s41467-021-21900-2. PubMed DOI PMC

Shen Y.-Y., Liang L., Zhu Z.-H., Zhou W.-P., Irwin D.M., Zhang Y.-P., Hillis D.M. Adaptive evolution of energy metabolism genes and the origin of flight in bats. PNAS. 2010;107:8666–8671. doi: 10.1073/pnas.0912613107. PubMed DOI PMC

Subudhi S., Rapin N., Misra V. Immune System Modulation and Viral Persistence in Bats: Understanding Viral Spillover. Viruses. 2019;11:192. doi: 10.3390/v11020192. PubMed DOI PMC

Banerjee A., Baker M.L., Kulcsar K., Misra V., Plowright R., Mossman K. Novel Insights into Immune Systems of Bats. Front. Immunol. 2020;11:26. doi: 10.3389/fimmu.2020.00026. PubMed DOI PMC

Begeman L., Suu-Ire R., Banyard A.C., Drosten C., Eggerbauer E., Freuling C.M., Gibson l., Goharriz H., Horton D.L., Jennings D., et al. Experimental Lagos bat virus infection in straw-colored fruit bats: A suitable model for bat rabies in a natural reservoir species. PLoS Negl. Trop. Dis. 2020;14:e0008898. doi: 10.1371/journal.pntd.0008898. PubMed DOI PMC

Irving A.T., Ahn M., Goh G., Anderson D.E., Wang L.F. Lessons from the host defences of bats, a unique viral reservoir. Nature. 2021;589:363–370. doi: 10.1038/s41586-020-03128-0. PubMed DOI

Brook C.E., Dobson A.P. Bats as ‘special’ reservoirs for emerging zoonotic pathogens. Trends Microbiol. 2015;23:172–180. doi: 10.1016/j.tim.2014.12.004. PubMed DOI PMC

Hayman D.T.S. Bats as viral reservoirs. Annu. Rev. Virol. 2016;3:77–99. doi: 10.1146/annurev-virology-110615-042203. PubMed DOI

Latinne A., Hu B., Olival K.J., Zhu G., Zhang L., Li H., Chmura A.A., Field H.E., Zambrana-Torrelio C., Epstein J.H., et al. Origin and cross-species transmission of bat coronaviruses in China. Nat. Commun. 2020;11:4235. doi: 10.1038/s41467-020-17687-3. PubMed DOI PMC

EUROBATS . Action Plan for the Conservation of Bat Species in the European Union 2016–2021. EUROBATS; Bonn, Germany: 2006. Inf.EUROBATS.AC21.5.

Teeling E.C., Springer M.S., Madsen O., Bates P., O’Brien S.J., Murphy W.J. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science. 2005;307:580–584. doi: 10.1126/science.1105113. PubMed DOI

Kohl C., Kurth A. European bats as carriers of viruses with zoonotic potential. Viruses. 2014;6:3110–3128. doi: 10.3390/v6083110. PubMed DOI PMC

Smreczak M., Orłowska A., Marzec A., Trębas P., Müller T., Freuling C.M., Żmudziński J.F. Bokeloh bat lyssavirus isolation in a Natterer’s bat, Poland. Zoonoses Public Health. 2018;65:1015–1019. doi: 10.1111/zph.12519. PubMed DOI

Vos A., Kaipf I., Denzinger A., Fooks A.R., Johnson N., Müller T. European bat lyssaviruses—An ecological enigma. Acta Chiropt. 2007;9:283–296. doi: 10.3161/1733-5329(2007)9[283:EBLAEE]2.0.CO;2. DOI

Banyard A.C., Hayman D., Johnson N., McElhinney L., Fooks A.R. Bats and lyssaviruses. Adv. Virus Res. 2011;79:239–289. doi: 10.1016/B978-0-12-387040-7.00012-3. PubMed DOI

Banyard A.C., Davis A., Gilbert A., Markotter W. Bat Rabies. In: Fooks A.R., Jackson A.C., editors. Rabies: Scientific Basis of the Disease and Its Management. 4th ed. Elsevier; Amsterdam, The Netherlands: 2020. pp. 231–276. Chapter 7.

Afonso C.L., Amarasinghe G.K., Bányai K., Bào Y., Basler C.F., Bavari S., Bejerman N., Blasdell K.R., Briand F.X., Briese T., et al. Taxonomy of the order Mononegavirales: Update 2016. Arch Virol. 2016;161:2351–2360. doi: 10.1007/s00705-016-2880-1. PubMed DOI PMC

Nokireki T., Tammiranta N., Kokkonen U.M., Kantala T., Gadd T. Tentative novel lyssavirus in a bat in Finland. Transbound. Emerg. Dis. J. 2018;65:593–596. doi: 10.1111/tbed.12833. PubMed DOI

Kuhn J.H., Adkins S., Agwanda B.R., Al Kubrusli R., Alkhovsky S.V., Amarasinghe G.K., Avšič-Županc T., Ayllón M.A., Bahl J., Balkema-Buschmann A., et al. Taxonomic update of phylum Negarnaviricota (Riboviria: Orthornavirae), including the large orders Bunyavirales and Mononegavirales. Arch Virol. 2021;166:3513–3566. doi: 10.1007/s00705-021-05143-6. PubMed DOI PMC

Coertse J., Markotter W., Le Roux K., Stewart D., Sabeta C.T., Nel L.H. New isolations of the rabies related Mokola virus from South Africa. BMC Vet. Res. 2017;13:37. doi: 10.1186/s12917-017-0948-0. PubMed DOI PMC

Klein A., Calvelage S., Schlottau K., Hoffmann B., Eggerbauer E., Müller T., Freuling C.M. Retrospective Enhanced Bat Lyssavirus Surveillance in Germany between 2018–2020. Viruses. 2021;13:1538. doi: 10.3390/v13081538. PubMed DOI PMC

Marston D.A., Horton D.L., Ngeleja C., Hampson K., McElhinney L.M., Banyard A.C., Haydon D., Cleaveland S., Rupprecht C.E., Bigambo M., et al. Ikoma lyssavirus, highly divergent novel lyssavirus in an African civet. Emerg. Infect. Dis. 2012;18:664–667. doi: 10.3201/eid1804.111553. PubMed DOI PMC

Markotter W., Kgaladi J., Nel L.H., Marston D., Wright N., Coertse J., Müller T.F., Sabeta C.T., Fooks A.R., Freuling C.M. Diversity and Epidemiology of Mokola Virus. PLoS Negl. Trop. Dis. 2013;7:e2511. PubMed PMC

Sabeta C.T., Markotter W., Mohale D.K., Shumba W., Wandeler A.I., Nel L.H. Mokola virus in domestic mammals, South Africa. Emerg. Infect. Dis. 2007;13:1371–1373. doi: 10.3201/eid1309.070466. PubMed DOI PMC

Rupprecht C., Kuzmin I., Meslin F. Lyssaviruses and rabies: Current conundrums, concerns, contradictions and controversies. F1000Research. 2017;6:184. doi: 10.12688/f1000research.10416.1. PubMed DOI PMC

Hu S., Hsu C., Lee M., Tu Y., Chang J., Wu C., Lee S.-H., Ting L.-J., Tsai K.-R., Cheng M.-C., et al. Lyssavirus in Japanese Pipistrelle, Taiwan. Emerg. Infect. Dis. 2018;24:782–785. doi: 10.3201/eid2404.171696. PubMed DOI PMC

Calvelage S., Tammiranta N., Nokireki T., Gadd T., Eggerbauer E., Zaeck L.M., Potratz M., Wylezich C., Höper D., Müller T., et al. Genetic and Antigenetic Characterization of the Novel Kotalahti Bat Lyssavirus (KBLV) Viruses. 2021;13:69. doi: 10.3390/v13010069. PubMed DOI PMC

Hu S.-C., Hsu C.-L., Lee F., Tu Y.-C., Chen Y.-W., Chang J.-C., Hsu W.-C. Novel Bat Lyssaviruses Identified by Nationwide Passive Surveillance in Taiwan, 2018–2021. Viruses. 2022;14:1562. doi: 10.3390/v14071562. PubMed DOI PMC

Coertse J., Grobler C.S., Sabeta C.T., Seamark E.C.J., Kearney T., Paweska J.T., Markotter W. Lyssaviruses in Insectivorous Bats, South Africa, 2003-2018. Emerg. Infect. Dis. 2020;26:3056–3060. doi: 10.3201/eid2612.203592. PubMed DOI PMC

Černe D., Hostnik P., Toplak I., Presetnik P., Maurer-Wernig J., Kuhar U. Discovery of a novel bat lyssavirus in a Long-fingered bat (Myotis capaccinii) from Slovenia. PLoS Negl Trop Dis. 2023;17:e0011420. doi: 10.1371/journal.pntd.0011420. PubMed DOI PMC

Serra-Cobo J., Amengual B., Abellan C., Bourhy H. European bat Lyssavirus infection in Spanish bat populations. Emerg. Infect. Dis. 2002;8:413–420. doi: 10.3201/eid0804.010263. PubMed DOI PMC

Picard-Meyer E., Dubourg-Savage M.J., Arthur L., Barataud M., Bécu D., Bracco S., Borel C., Larcher G., Meme-Lafond B., Moinet M., et al. Active surveillance of bat rabies in France: A 5-year study (2004–2009) Vet Microbiol. 2011;151:390–395. doi: 10.1016/j.vetmic.2011.03.034. PubMed DOI

Schatz J., Fooks A.R., McElhinney L., Horton D., Echevarria J., Vázquez-Moron S., Kooi E.A., Rasmussen T.B., Müller T., Freuling C.M. Bat rabies surveillance in Europe. Zoonoses Public Health. 2012;60:22–34. doi: 10.1111/zph.12002. PubMed DOI

Mingo-Casas P., Sandonis V., Obón E., Berciano J.M., Vázquez-Morón S., Juste J., Echevarria J.E. First cases of European bat lyssavirus type 1 in Iberian serotine bats: Implications for the molecular epidemiology of bat rabies in Europe. PLoS Negl Trop Dis. 2018;12:e0006290. doi: 10.1371/journal.pntd.0006290. PubMed DOI PMC

Echevarria J.E., Avellon A., Juste J., Vera M., Ibayez C. Screening of active lyssavirus infection in wild bat populations by viral RNA on oropharyngeal swabs. J. Clin. Microbiol. 2001;39:3678–3683. doi: 10.1128/JCM.39.10.3678-3683.2001. PubMed DOI PMC

Davis P.L., Holmes E.C., Larrous F., Van der Poel W.H., Tjørnehøj K., Alonso W.J., Bourhy H. Phylogeography, population dynamics, and molecular evolution of European bat lyssaviruses. Virol. J. 2005;79:10487–10497. doi: 10.1128/JVI.79.16.10487-10497.2005. PubMed DOI PMC

Dacheux L., Larrous F., Mailles A., Boisseleau D., Delmas O., Biron C., Bouchier C., Capek I., Muller M., Ilari F., et al. European Bat Lyssavirus Transmission among Cats, Europe. Emerg. Infect. Dis. 2009;15:280–284. doi: 10.3201/eid1502.080637. PubMed DOI PMC

Muller T., Cox J., Peter W., Schafer R., Johnson N., McElhinney L.M., Geue J.L., Tjornehoj K., Fooks A.R. Spill-over of European bat lyssavirus type 1 into a stone marten (Martes foina) in Germany. J. Vet. Med. Ser. B. 2004;51:49–54. doi: 10.1111/j.1439-0450.2003.00725.x. PubMed DOI

Tjørnehøj K., Fooks A.R., Agerholm J.S., Rønsholt L. Natural and experimental infection of sheep with European bat lyssavirus type-1 of Danish bat origin. J. Comp. Pathol. 2006;134:190–201. doi: 10.1016/j.jcpa.2005.10.005. PubMed DOI

Schatz J., Freuling C.M., Auer E., Goharriz H., Harbusch C., Johnson N., Kaipf I., Mettenleiter T.C., Mühldorfer K., Mühle R.-U., et al. Enhanced Passive Bat Rabies Surveillance in Indigenous Bat Species from Germany—A Retrospective Study. PLoS Negl. Trop Dis. 2014;8:e2835. doi: 10.1371/journal.pntd.0002835. PubMed DOI PMC

Megali A., Yannic G., Zahno M.L., Brügger D., Bertoni G., Christe P., Zanoni R. Surveillance for European bat lyssavirus in Swiss bats. Arch Virol. 2010;155:1655–1662. doi: 10.1007/s00705-010-0750-9. PubMed DOI

Fooks A.R., McElhinney L.M., Pounder D.J., Finnegan C.J., Mansfield K., Johnson N., Brookes S.M., Parsons G., White K., McIntyre P.G., et al. Case Report: Isolation of a European Bat Lyssavirus Type 2a From a Fatal Human Case of Rabies Encephalitis. J. Med. Virol. 2003;71:281–289. doi: 10.1002/jmv.10481. PubMed DOI

Müller T., Johnson N., Freuling C.M., Fooks A.R., Selhorst T., Vos A. Epidemiology of bat rabies in Germany. Arch Virol. 2007;152:273–288. doi: 10.1007/s00705-006-0853-5. PubMed DOI

Amengual B., Whitby J.E., King A., Cobo J.S., Bourhy H. Evolution of European bat lyssaviruses. J. Gen. Virol. 1997;78:2319–2328. doi: 10.1099/0022-1317-78-9-2319. PubMed DOI

Freuling C.M., Beer M., Conraths F.J., Finke S., Hoffmann B., Keller B., Kliemt J., Mettenleiter T.C., Mühlbach E., Teifke J.P., et al. Novel lyssavirus in natterer’s bat, Germany. Emerg. Infect. Dis. 2011;17:1519–1522. doi: 10.3201/eid1708.110201. PubMed DOI PMC

Picard-Meyer E., Servat A., Robardet E., Moinet M., Borel C., Cliquet F. Isolation of Bokeloh bat lyssavirus in Myotis nattereri in France. Arch. Virol. 2013;158:2333–2340. doi: 10.1007/s00705-013-1747-y. PubMed DOI

Puechmaille S.J., Allegrini B., Boston E.S., Dubourg-Savage M.-J., Evin A., Knochel A., Le Bris Y., Lecoq V., Lemaire M., Rist D., et al. Genetic analyses reveal further cryptic lineages within the Myotis nattereri species complex. Mamm. Biol. 2012;77:224–228. doi: 10.1016/j.mambio.2011.11.004. DOI

Coxon C., McElhinney L., Pacey A., Gauntlett F., Holland S. Preliminary Outbreak Assessment: Rabies in a Cat in Italy. Department for Environment, Food and Rural Affairs, Animal and Plant Health Agency, Advice Services—International Disease Monitoring. [(accessed on 8 August 2023)];2020 Available online: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/897070/rabies-cat-italy-poa.pdf.

Van Der Poel W.H.M., Van Der Heide R., Van Amerongen G., Van Keulen L.J.M., Wellenberg G.J., Bourhy H., Schaftenaar W., Groen J., Osterhaus A.D.M.E. Characterisation of a recently isolated lyssavirus in frugivorous zoo bats. Arch. Virol. 2000;145:1919–1931. doi: 10.1007/s007050070066. PubMed DOI

Nel L.H., Rupprecht C.E. Emergence of lyssaviruses in the Old World: The case of Africa. Curr. Top. Microbiol. Immunol. 2007;315:161–193. doi: 10.1007/978-3-540-70962-6_8. PubMed DOI

Hayman D.T.S., Fooks A.R., Marston D.A., Garcia-R J.C. The Global Phylogeography of Lyssaviruses—Challenging the ‘Out of Africa’ Hypothesis. PLoS Negl. Trop. Dis. 2016;10:e0005266. doi: 10.1371/journal.pntd.0005266. PubMed DOI PMC

Longdon B., Murray G.G., Palmer W.J., Day J.P., Parker D.J., Welch J.J., Obbard D.J., Jiggins F.M. The evolution, diversity, and host associations of rhabdoviruses. Virus Evol. 2015;1:vev014. doi: 10.1093/ve/vev014. PubMed DOI PMC

Li C.X., Shi M., Tian J.H., Lin X.D., Kang Y.J., Chen L., Qin X.C., Xu J., Holmes E.C., Zhang Y.Z. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife. 2015;29:e05378. doi: 10.7554/eLife.05378. PubMed DOI PMC

Walker P.J., Firth C., Widen S.G., Blasdell K.R., Guzman H., Wood T.G., Paradkar P.N., Holmes E., Tesh R.B., Vasilakis N. Evolution of genome size and complexity in the Rhabdoviridae. PLoS Pathog. 2015;11:e1004664. doi: 10.1371/journal.ppat.1004664. PubMed DOI PMC

Velasco-Villa A., Mauldin M.R., Shi M., Escobar L.E., Gallardo-Romero N.F., Damon I., Olson V.A., Streicker D.G., Emerson G. The history of rabies in the Western Hemisphere. Antivir. Res. 2017;146:221–232. doi: 10.1016/j.antiviral.2017.03.013. PubMed DOI PMC

Caraballo D.A., Lema C., Novaro L., Gury-Dohmen F., Russo S., Beltrán F.J., Palacios G., Cisterna D.M. A Novel Terrestrial Rabies Virus Lineage Occurring in South America: Origin, Diversification, and Evidence of Contact between Wild and Domestic Cycles. Viruses. 2021;13:2484. doi: 10.3390/v13122484. PubMed DOI PMC

Singh R., Singh K.P., Cherian S., Saminathan M., Kapoor S., Manjunatha Reddy G.B., Panda S., Dhama K. Rabies–epidemiology, pathogenesis, public health concerns and advances in diagnosis and control: A comprehensive review. Vet. Q. 2017;37:212–251. doi: 10.1080/01652176.2017.1343516. PubMed DOI

Potratz M., Zaeck L.M., Weigel C., Klein A., Freuling C.M., Müller T., Finke S. Neuroglia infection by rabies virus after anterograde virus spread in peripheral neurons. ANC. 2020;8:1–15. doi: 10.1186/s40478-020-01074-6. PubMed DOI PMC

Baghi H.B., Rupprecht C. Notes on three periods of rabies focus in the Middle East: From progress during the cradle of civilization to neglected current history. Zoonoses Public Health. 2021;68:697–703. doi: 10.1111/zph.12781. PubMed DOI

Badrane H., Tordo N. Host switching in Lyssavirus history from the chiroptera to the carnivora orders. J. Virol. 2001;75:8096–8104. doi: 10.1128/JVI.75.17.8096-8104.2001. PubMed DOI PMC

Rupprecht C.E., Turmelle A., Kuzmin I.V. A perspective on lyssavirus emergence and perpetuation. COVIRO. 2011;1:662–670. doi: 10.1016/j.coviro.2011.10.014. PubMed DOI

Badrane H., Bahloul C., Perrin P., Tordo N. Evidence of two Lyssavirus phylogroups with distinct pathogenicity and immunogenicity. Virol. J. 2001;75:3268–3276. doi: 10.1128/JVI.75.7.3268-3276.2001. PubMed DOI PMC

Fooks A., Brookes S., Johnson N., McElhinney L., Hutson A. European bat lyssaviruses: An emerging zoonosis. Epidemiol. Infect. 2003;131:1029–1039. doi: 10.1017/S0950268803001481. PubMed DOI PMC

McElhinney L.M., Marston D.A., Wise E.L., Freuling C.M., Bourhy H., Zanoni R., Moldal T., Kooi E.A., Neubauer-Juric A., Nokireki T., et al. Molecular Epidemiology and Evolution of European Bat Lyssavirus 2. Int. J. Mol. Sci. 2018;19:156. doi: 10.3390/ijms19010156. PubMed DOI PMC

Šimić I., Lojkić I., Krešić N., Cliquet F., Picard-Meyer E., Wasniewski M., Ćukušić A., Zrnčić V., Bedeković T. Molecular and serological survey of lyssaviruses in Croatian bat populations. BMC Vet. Res. 2018;14:274. doi: 10.1186/s12917-018-1592-z. PubMed DOI PMC

Seidlova V., Zukal J., Brichta J., Anisimov N., Apoznański G., Bandouchova H., Bartonička T., Berková H., Botvinkin A.D., Heger T., et al. Active surveillance for antibodies confirms circulation of lyssaviruses in Palearctic bats. BMC Vet. Res. 2020;16:482. doi: 10.1186/s12917-020-02702-y. PubMed DOI PMC

Kuzmin I.V., Hughes G.J., Botvinkin A.D., Orciari L.A., Rupprecht C.E. Phylogenetic relationships of Irkut and West Caucasian bat viruses within the Lyssavirus genus and suggested quantitative criteria based on the N gene sequence for lyssavirus genotype definition. Virus Res. 2005;111:28–43. doi: 10.1016/j.virusres.2005.03.008. PubMed DOI

Ceballos N., Morón S., Berciano J.M., Nicolás O., López C., Juste J., Nevado C., Setién A.A., Echevarría J.E. Novel Lyssavirus in Bat, Spain. Emerg Infect Dis. 2013;19:793–795. doi: 10.3201/eid1905.121071. PubMed DOI PMC

Jakava-Viljanen M., Nokireki T., Sironen T., Vapalahti O., Sihvonen L., Liisa S., Huovilainen A. Evolutionary trends of European bat lyssavirus type 2 including genetic characterization of Finnish strains of human and bat origin 24 years apart. Arch. Virol. 2015;160:1489–1498. doi: 10.1007/s00705-015-2475-2. PubMed DOI PMC

Harris S.L., Aegerter J.N., Brookes S.M., McElhinney L.M., Jones G., Smith G.C., Fooks A.R. Targeted surveillance for European bat lyssaviruses in English bats (2003-06) J. Wildl. Dis. 2009;45:1030–1041. doi: 10.7589/0090-3558-45.4.1030. PubMed DOI

Dietzgen R.G., Kondo H., Goodin M.M., Kurath G., Vasilakis N. The family Rhabdoviridae: Mono- and bipartite negative-sense RNA viruses with diverse genome organization and common evolutionary origins. Virus Res. 2017;227:158–170. doi: 10.1016/j.virusres.2016.10.010. PubMed DOI PMC

Lelli D., Prosperi A., Moreno A., Chiapponi C., Gibellini A.M., De Benedictis P., Leopardi S., Sozzi E., Lavazza A. Isolation of a novel Rhabdovirus from an insectivorous bat (Pipistrellus kuhlii) in Italy. Virol. J. 2018;15:1–7. doi: 10.1186/s12985-018-0949-z. PubMed DOI PMC

Walker P.J., Dietzgen R.G., Joubert D.A., Blasdell K.R. Rhabdovirus accessory genes. Virus Res. 2011;162:110–125. doi: 10.1016/j.virusres.2011.09.004. PubMed DOI PMC

Kuzmin I.V., Wu X., Tordo N., Rupprecht C.E. Complete genomes of Aravan, Khujand, Irkut and West Caucasian bat viruses, with special attention to the polymerase gene and non-coding regions. Virus Res. 2008;136:81–90. doi: 10.1016/j.virusres.2008.04.021. PubMed DOI

Kuzmin I.V., Orciari L.A., Arai Y.T., Smith J.S., Hanlon C.A., Kameoka Y., Rupprecht C.E. Bat lyssaviruses (Aravan and Khujand) from Central Asia: Phylogenetic relationships according to N, P and G gene sequences. Virus Res. 2003;97:65–79. doi: 10.1016/S0168-1702(03)00217-X. PubMed DOI

Kuzmin I.V., Novella I.S., Dietzgen R.G., Padhi A., Rupprecht C.E. The rhabdoviruses: Biodiversity, phylogenetics, and evolution. Infect Genet Evol. 2009;9:541–553. doi: 10.1016/j.meegid.2009.02.005. PubMed DOI

Delmas O., Holmes E.C., Talbi C., Larrous F., Dacheux L., Bouchier C., Bourhy H. Genomic diversity and evolution of the lyssaviruses. PLoS ONE. 2008;3:e2057. doi: 10.1371/journal.pone.0002057. PubMed DOI PMC

Fooks A.R., Cliquet F., Finke S., Freuling C., Hemachudha T., Mani R.S., Müller T., Nadin-Davis S., Picard-Meyer E., Wilde H., et al. Rabies. Nat. Rev. Dis. Prim. 2017;3:17091. doi: 10.1038/nrdp.2017.91. PubMed DOI

Vega S., Lorenzo-Rebenaque L., Marin C., Domingo R., Fariñas F. Tackling the Threat of Rabies Reintroduction in Europe. Front. Vet. Sci. 2021;7:613712. doi: 10.3389/fvets.2020.613712. PubMed DOI PMC

Gunawardena P.S., Marston D.A., Ellis R.J., Wise E.L., Karawita A.C., Breed A.C., Fooks A.R. Lyssavirus in Indian flying foxes Sri Lanka. Emerg. Infect. Dis. 2016;22:1456–1459. doi: 10.3201/eid2208.151986. PubMed DOI PMC

Kuzmin I.V., Mayer A.E., Niezgoda M., Markotter W., Agwanda B., Breiman R.F., Rupprecht C.E. Shimoni bat virus, a new representative of the Lyssavirus genus. Virus Res. 2010;149:197–210. doi: 10.1016/j.virusres.2010.01.018. PubMed DOI

Tordo N., Poch O., Ermine A., Keith G., Rougeon F. Completion of the rabies virus genome sequence determi-nation: Highly conserved domains among the L (polymerase) proteins of unsegmented negative-strand RNA viruses. Virology. 1988;165:565–576. doi: 10.1016/0042-6822(88)90600-9. PubMed DOI

Gould A.R., Kattenbelt J.A., Gumley S.G., Lunt R.A. Characterisation of an Australian bat lyssavirus variant isolated from an insectivorous bat. Virus Res. 2002;89:1–28. doi: 10.1016/S0168-1702(02)00056-4. PubMed DOI

Marston D.A., McElhinney L.M., Johnson N., Müller T., Conzelmann K.K., Tordo N., Fooks A.R. Comparative analysis of the full genome sequence of European bat lyssavirus type 1 and type 2 with other lyssaviruses and evidence for a conserved transcription termination and polyadenylation motif in the G-L 3’ non-translated region. J. Gen. Virol. 2007;88:1302–1314. doi: 10.1099/vir.0.82692-0. PubMed DOI

Le Mercier P., Jacob Y., Tordo N. The complete Mokola virus genome sequence: Structure of the RNA-dependent RNA polymerase. J. Gen. Virol. 1997;78:1571–1576. doi: 10.1099/0022-1317-78-7-1571. PubMed DOI

Nei M., Kumar S. Molecular Evolution and Phylogenetics. Oxford University Press; New York, NY, USA: 2000.

Kumar S., Stecher G., Li M., Knyaz C., Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC

Kuzmin I.V., Bozick B., Guagliardo S.A., Kunkel R., Shak J.R., Tong S., Rupprecht C.E. Bats, emerging infectious diseases, and the rabies paradigm revisited. Emerg. Health. Threats. J. 2011;4:1. doi: 10.3402/ehtj.v4i0.7159. PubMed DOI PMC

Kuzmin I.V., Rupprecht C.E. Bats and Viruses: A New Frontier of Emerging Infectious Diseases. John Wiley and Sons, Inc.; Hoboken, NJ, USA: 2015. Bat Lyssaviruses; pp. 47–97. DOI

Dietz C., von Helversen O., Nill D. Bats of Britain. Europe and Northwest Africa. A and C Black; London, UK: 2009. 400p

Arnaout Y., Djelouadji Z., Robardet E., Cappelle J., Cliquet F., Touzalin F., Jimenez G., Hurstel S., Borel C., Picard-Meyer E. Genetic identification of bat species for pathogen surveillance across France. PLoS ONE. 2022;4:e0261344. doi: 10.1371/journal.pone.0261344. PubMed DOI PMC

Çoraman E., Dundarova H., Dietz C., Mayer F. Patterns of mtDNA introgression suggest population replacement in Palaearctic whiskered bat species. R. Soc. Open Sci. 2020;7:191805. doi: 10.1098/rsos.191805. PubMed DOI PMC

De Benedictis P., Leopardi S., Markotter W., Velasco-Villa A. The Importance of Accurate Host Species Identification in the Framework of Rabies Surveillance, Control and Elimination. Viruses. 2022;14:492. doi: 10.3390/v14030492. PubMed DOI PMC

Parize P., Travecedo Robledo I.C., Cervantes-Gonzalez M., Kergoat L., Larrous F., Serra-Cobo J., Dacheux L., Bourhy H. Circumstances of Human–Bat interactions and risk of lyssavirus transmission in metropolitan France. Zoonoses Public Health. 2020;67:774–784. doi: 10.1111/zph.12747. PubMed DOI

Salicini I., Ibáñez C., Juste J. Multilocus phylogeny and species delimitation within the Natterer’s bat species complex in the Western Palearctic. Mol. Phylogenet. Evol. 2011;61:888–898. doi: 10.1016/j.ympev.2011.08.010. PubMed DOI

Salicini I., Ibáñez C., Juste J. Deep differentiation between and within Mediterranean glacial refugia in a flying mammal, the Myotis nattereri bat complex. J. Biogeogr. 2013;40:1182–1193. doi: 10.1111/jbi.12062. DOI

Eggerbauer E., Troupin C., Passior K., Pfaff F., Höper D., Neubauer-Juric A., Haberl S., Bouchier C., Mettenleiter T.C., Bourhy H., et al. The Recently Discovered Bokeloh Bat Lyssavirus: Insights Into Its Genetic Heterogeneity and Spatial Distribution in Europe and the Population Genetics of Its Primary Host. Adv. Virus Res. 2017;99:199–232. doi: 10.1016/bs.aivir.2017.07.004. PubMed DOI

Çoraman E., Dietz C., Hempel E., Ghazaryan A., Levin E., Presetnik P., Zagmajster M., Mayer F. Reticulate evolutionary history of a Western Palaearctic Bat Complex explained by multiple mtDNA introgressions in secondary contacts. J. Biogeogr. 2019;46:343–354. doi: 10.1111/jbi.13509. DOI

Fooks A.R., Shipley R., Markotter W., Tordo N., Freuling C.M., Müller T., McElhinney L.M., Banyard A.C., Rupprecht C.E. Renewed Public Health Threat from Emerging Lyssaviruses. Viruses. 2021;13:1769. doi: 10.3390/v13091769. PubMed DOI PMC

Wright P.G.R., Newton J., Agnelli P., Budinski I., Salvo I.D., Flaquer C., Fulco A., Georgiakakis P., Martinoli A., Mas M., et al. Hydrogen isotopes reveal evidence of migration of Miniopterus schreibersii in Europe. BMC Ecolol. 2020;20:52. doi: 10.1186/s12898-020-00321-7. PubMed DOI PMC

Freuling C., Vos A., Johnson N., Kaipf I., Denzinger A., Neubert L., Mansfield K., Hicks D., Nuñez A., Tordo N., et al. Experimental infection of serotine bats (Eptesicus serotinus) with European bat lyssavirus type 1a. J. Gen. Virol. 2009;90:2493–2502. doi: 10.1099/vir.0.011510-0. PubMed DOI

de Thoisy B., Bourhy H., Delaval M., Pontier D., Dacheux L., Darcissac E., Donato D., Guidez A., Larrous F., Lavenir R., et al. Bioecological drivers of rabies virus circulation in a neotropical bat community. PLoS Negl. Trop. Dis. 2016;10:e0004378. doi: 10.1371/journal.pntd.0004378. PubMed DOI PMC

Bonnaud E.M., Troupin C., Dacheux L., Holmes E.C., Monchatre-Leroy E., Tanguy M., Bouchier C., Cliquet F., Barrat J., Bourhy H. Comparison of intra-and inter-host genetic diversity in rabies virus during experimental cross-species transmission. PLoS Pathog. 2019;15:e1007799. doi: 10.1371/journal.ppat.1007799. PubMed DOI PMC

Colombi D., Serra-Cobo J., Métras R., Apolloni A., López-Roig M., Bourhy H., Colizza V. Mechanisms for lyssavirus persistence in non-synanthropic bats in Europe: Insights from a modelling study. Sci. Rep. 2019;9:537. doi: 10.1038/s41598-018-36485-y. PubMed DOI PMC

Horton D.L., Breed A.C., Arnold M.E., Smith G.C., Aegerter J.N., McElhinney L.M., Johnson N., Banyard A.C., Raynor R., Mackie I., et al. Between roost contact is essential for maintenance of European bat lyssavirus type-2 in Myotis daubentonii bat reservoir: ‘The Swarming Hypothesis’. Sci. Rep. 2020;10:1740. doi: 10.1038/s41598-020-58521-6. PubMed DOI PMC

Tájek P., Tájková P. A long distance migration in Nyctalus leisleri from the Czech Republic to southern France (Chiroptera: Vespertilionidae) Lynx Ser. Nova. 2020;51:223–226. doi: 10.37520/lynx.2020.016. DOI

Dundarova H., Michev B., Pandourski I. Bats over the Western Black Sea open water area. Acta Zool. Bulg. 2021;73:543–546.

Bouma H.R., Carey H.V., Kroese F.G. Hibernation: The immune system at rest? J. Leukoc. Biol. 2010;88:619–624. doi: 10.1189/jlb.0310174. PubMed DOI

Field K.A., Sewall B.J., Prokkola J.M., Turner G.G., Gagnon M.F., Liley T.M., White J.P., Johnson J.J., Hauer C.L., Reeder D.M. Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats. Mol. Ecol. 2018;27:3727–3743. doi: 10.1111/mec.14827. PubMed DOI

Constantine D.G. Bat Rabies and Other Lyssavirus Infections. US Geological Survey; Reston, VA, USA: 2009. 68p

Harazim M., Perrot J., Varet H., Bourhy H., Lannoy J., Pikula J., Seidlová V., Dacheux M., Martínková N. Transcriptomic responses of bat cells to European bat lyssavirus 1 infection under conditions simulating euthermia and hibernation. BMC Immunol. 2023;24:7. doi: 10.1186/s12865-023-00542-7. PubMed DOI PMC

Gilbert A.T., McCracken G.F., Sheeler L.L., Muller L.I., O’Rourke D., Kelch W.J., New J.C., Jr. Rabies surveillance among bats in Tennessee, USA, 1996–2010. J. Wildl. Dis. 2015;51:821–832. doi: 10.7589/2014-12-277. PubMed DOI

Robardet E., Borel C., Moinet M., Jouan D., Wasniewski M., Barrat J., Boué F., Montchâtre-Leroy E., Servat A., Gimenez O., et al. Longitudinal survey of two serotine bat (Eptesicus serotinus) maternity colonies exposed to EBLV-1 (European Bat Lyssavirus type 1): Assessment of survival and serological status variations using capture-recapture models. PLoS Negl. Trop. Dis. 2017;11:e0006048. doi: 10.1371/journal.pntd.0006048. PubMed DOI PMC

Shipley R., Wright E., Selden D., Wu G., Aegerter J., Fooks A.R., Banyard A.C. Bats and viruses: Emergence of novel lyssaviruses and association of bats with viral zoonoses in the EU. Infect. Dis. Trop. Med. 2019;4:31. doi: 10.3390/tropicalmed4010031. PubMed DOI PMC

Constantine D.G., Emmons R.W., Woodie J.D. Rabies virus in nasal mucosa of naturally infected bats. Science. 1972;175:1255–1256. doi: 10.1126/science.175.4027.1255. PubMed DOI

Allendorf S.D., Cortez A., Heinemann M.B., Harary C.M.A., Antunes J.M.A., Peres M.G., Vicente A.F., Sodré M.M., da Rosa R., Megid J. Rabies virus distribution in tissues and molecular characterization of strains from naturally infected non-hematophagous bats. Virus Res. 2012;165:119–125. doi: 10.1016/j.virusres.2012.01.011. PubMed DOI

Fisher C.R., Streicker D.G., Schnell M.J. The spread and evolution of rabies virus: Conquering new frontiers. Nat. Rev. Microbiol. 2018;16:241–255. doi: 10.1038/nrmicro.2018.11. PubMed DOI PMC

Davis A., Rudd R.J., Bowen R.A. Effects of Aerosolized Rabies Virus Exposure on Bats and Mice. J. Infect. Dis. 2007;195:151144–151150. doi: 10.1086/512616. PubMed DOI

Johnson N., Phillpotts R., Fooks A.R. Airborne transmission of lyssaviruses. J. Med. Microbiol. 2006;55:785–790. doi: 10.1099/jmm.0.46370-0. PubMed DOI

Lojkić I., Šimić I., Bedeković T., Krešić N. Current Status of Rabies and Its Eradication in Eastern and Southeastern Europe. Pathogens. 2021;10:742. doi: 10.3390/pathogens10060742. PubMed DOI PMC

Leopardi S., Barneschi E., Manna G., Zecchin B., Priori P., Drzewnioková P., Festa F., Lombardo A., Parca F., Scaravelli D., et al. Spillover of West Caucasian Bat Lyssavirus (WCBV) in a Domestic Cat and Westward Expansion in the Palearctic Region. Viruses. 2021;13:2064. doi: 10.3390/v13102064. PubMed DOI PMC

Banyard A.C., Evans J.S., Luo T.R., Fooks A.R. Lyssaviruses and bats: Emergence and zoonotic threat. Viruses. 2014;6:2974–2990. doi: 10.3390/v6082974. PubMed DOI PMC

Kuzmin I.V., Niezgoda M., Franka R., Agwanda B., Markotter W., Beagley J.C., Urazova O.Y., Breiman R.F., Rupprecht C.E. Lagos bat virus in Kenya. J. Clin. Microbio. 2008;46:1451–1461. doi: 10.1128/JCM.00016-08. PubMed DOI PMC

Kuzmin I.V., Turmelle A.S., Agwanda B., Markotter W., Niezgoda M., Breiman R.F., Rupprecht C.E. Commerson’s Leaf-Nosed Bat (Hipposideros commersoni) is the Likely Reservoir of Shimoni Bat Virus. Vector-Borne Zoonotic Dis. 2011;11:1465–1470. doi: 10.1089/vbz.2011.0663. PubMed DOI

Lučan R.K., Bartonička T., Benda P., Bilgin R., Jedlička P., Nicolaou H., Reiter A., Shohdi W.M., Šálek M., Řeřucha Š., et al. Reproductive seasonality of the Egyptian fruit bat (Rousettus aegyptiacus) at the northern limits of its distribution. J. Mammal. 2014;95:1036–1042. doi: 10.1644/14-MAMM-A-035. DOI

Benda P., Abi-Said M., Bartonička T., Bilgin R., Faizolahi K., Lučan R.K., Nicolaou H., Raiter A., Shohdi W.M., Uhrin M., et al. Rousettus aegyptiacus (Pteropodidae) in the Palaearctic: List of records and revision of the distribution range. Vespertilio. 2011;15:3–36.

Benda P., Abi Said M.R., Bou Jaoude I., Karanouh R., Lučan R.K., Sadek R., Ševčik M., Uhrin M., Horáček I. Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 13. Review of distribution and ectoparasites of bats in Lebanon. Acta Soc. Zool. Bohem. 2016;80:207–316.

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

Wang Z., Huang G., Huang M., Dai Q., Hu Y., Zhou J., Wei F. Global patterns of phylogenetic diversity and transmission of bat coronavirus. Sci. China Life Sci. 2022;66:861–874. doi: 10.1007/s11427-022-2221-5. PubMed DOI PMC

Albery G.F., Becker D.J., Brierley L., Brook C.E., Christofferson R.C., Cohen L.E., Dallas T.A., Eskew E.A., Fagre A., Farrell M.J., et al. The science of the host-virus network. Nat. Microbiol. 2021;6:1483–1492. doi: 10.1038/s41564-021-00999-5. PubMed DOI