{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T05:15:55Z","timestamp":1787030155954,"version":"build-2736575974"},"reference-count":78,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2021,5,8]],"date-time":"2021-05-08T00:00:00Z","timestamp":1620432000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007015","name":"University of Wisconsin-Madison","doi-asserted-by":"publisher","award":["Global Health Institute Graduate Research Award"],"award-info":[{"award-number":["Global Health Institute Graduate Research Award"]}],"id":[{"id":"10.13039\/100007015","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100007015","name":"University of Wisconsin-Madison","doi-asserted-by":"publisher","award":["John D. MacArthur Professorship Chair"],"award-info":[{"award-number":["John D. MacArthur Professorship Chair"]}],"id":[{"id":"10.13039\/100007015","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Universidad de Guadalajara","award":["none"],"award-info":[{"award-number":["none"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Bat flies (Hippoboscoidea: Nycteribiidae and Streblidae) are obligate hematophagous ectoparasites of bats. We collected streblid bat flies from the New World (M\u00e9xico) and the Old World (Uganda), and used metagenomics to identify their viruses. In M\u00e9xico, we found m\u00e9jal virus (Rhabdoviridae; Vesiculovirus), Amate virus (Reoviridae: Orbivirus), and two unclassified viruses of invertebrates. M\u00e9jal virus is related to emerging zoonotic encephalitis viruses and to the agriculturally important vesicular stomatitis viruses (VSV). Amate virus and its sister taxon from a bat are most closely related to mosquito- and tick-borne orbiviruses, suggesting a previously unrecognized orbivirus transmission cycle involving bats and bat flies. In Uganda, we found mamucuso virus (Peribunyaviridae: Orthobunyavirus) and two unclassified viruses (a rhabdovirus and an invertebrate virus). Mamucuso virus is related to encephalitic viruses of mammals and to viruses from nycteribiid bat flies and louse flies, suggesting a previously unrecognized orthobunyavirus transmission cycle involving hippoboscoid insects. Bat fly virus transmission may be neither strictly vector-borne nor strictly vertical, with opportunistic feeding by bat flies occasionally leading to zoonotic transmission. Many \u201cbat-associated\u201d viruses, which are ecologically and epidemiologically associated with bats but rarely or never found in bats themselves, may actually be viruses of bat flies or other bat ectoparasites.<\/jats:p>","DOI":"10.3390\/v13050860","type":"journal-article","created":{"date-parts":[[2021,5,10]],"date-time":"2021-05-10T02:54:58Z","timestamp":1620615298000},"page":"860","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":31,"title":["Bat Flies of the Family Streblidae (Diptera: Hippoboscoidea) Host Relatives of Medically and Agriculturally Important \u201cBat-Associated\u201d Viruses"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8705-1211","authenticated-orcid":false,"given":"Mar\u00eda M.","family":"Ram\u00edrez-Mart\u00ednez","sequence":"first","affiliation":[{"name":"Departamento de Ciencias de la Salud y Ecolog\u00eda Humana, Universidad de Guadalajara, Guadalajara, Autl\u00e1n CP 48900, Mexico"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew J.","family":"Bennett","sequence":"additional","affiliation":[{"name":"Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin\u2013Madison, Madison, WI 53706, USA"},{"name":"Genomics and Bioinformatics Department, Biological Defense Research Directorate, Naval Medical Research Center\u2013Frederick, Fort Detrick, Frederick, MD 21702, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christopher D.","family":"Dunn","sequence":"additional","affiliation":[{"name":"Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin\u2013Madison, Madison, WI 53706, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas M.","family":"Yuill","sequence":"additional","affiliation":[{"name":"Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin\u2013Madison, Madison, WI 53706, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3962-4913","authenticated-orcid":false,"given":"Tony L.","family":"Goldberg","sequence":"additional","affiliation":[{"name":"Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin\u2013Madison, Madison, WI 53706, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,5,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Morand, S., Krasnov, B.R., and Poulin, R. (2006). Bat flies: Obligate ectoparasites of bats. Micromammals and Macroparasites, Springer.","DOI":"10.1007\/978-4-431-36025-4"},{"key":"ref_2","first-page":"1283","article-title":"Nycteribiidae","volume":"Volume 2","author":"McAlpine","year":"1987","journal-title":"Manual of Nearctic Diptera"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"780","DOI":"10.11646\/zootaxa.4122.1.66","article-title":"Family Nycteribiidae","volume":"4122","author":"Graciolli","year":"2016","journal-title":"Zootaxa"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"784","DOI":"10.11646\/zootaxa.4122.1.67","article-title":"Family Streblidae","volume":"4122","author":"Dick","year":"2016","journal-title":"Zootaxa"},{"key":"ref_5","unstructured":"Morand, S., Krasnov, B.R., and Littlewood, T. (2015). Bat fly evolution from the Eocene to the present (Hippoboscoidea, Streblidae and Nycteribiidae). Parasite Diversity and Diversification: Evolutionary Ecology Meets Phylogenetics, Cambridge University Press."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1186\/s13071-016-1625-z","article-title":"Bat flies (Diptera: Nycteribiidae and Streblidae) infesting cave-dwelling bats in Gabon: Diversity, dynamics and potential role in Polychromophilus melanipherus transmission","volume":"9","author":"Rahola","year":"2016","journal-title":"Parasit. Vectors"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"591","DOI":"10.1017\/S0031182000080215","article-title":"Polychromophilus murinus: A malarial parasite of bats: Life-history and ultrastructural studies","volume":"96","author":"Gardner","year":"1988","journal-title":"Parasitology"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1717","DOI":"10.1016\/j.meegid.2012.06.009","article-title":"Global distribution and genetic diversity of Bartonella in bat flies (Hippoboscoidea, Streblidae, Nycteribiidae)","volume":"12","author":"Morse","year":"2012","journal-title":"Infect. Genet. Evol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1017\/S0031182011002113","article-title":"Bartonella species in bat flies (Diptera: Nycteribiidae) from western Africa","volume":"139","author":"Billeter","year":"2012","journal-title":"Parasitology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1089\/vbz.2018.2350","article-title":"Isolation and Identification of a highly divergent Kaeng Khoi virus from bat flies (Eucampsipoda sundaica) in China","volume":"19","author":"Xu","year":"2019","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1099\/jgv.0.000753","article-title":"Isolation of a novel orthobunyavirus from bat flies (Eucampsipoda africana)","volume":"98","author":"Wiley","year":"2017","journal-title":"J. Gen. Virol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.virusres.2017.06.007","article-title":"Isolation of Kaeng Khoi virus (KKV) from Eucampsipoda sundaica bat flies in China","volume":"238","author":"Feng","year":"2017","journal-title":"Virus Res."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Van Vuren, P.J., Wiley, M., Palacios, G., Storm, N., McCulloch, S., Markotter, W., Birkhead, M., Kemp, A., and Paweska, J.T. (2016). Isolation of a novel fusogenic orthoreovirus from Eucampsipoda africana bat flies in South Africa. Viruses, 8.","DOI":"10.3390\/v8030065"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Bennett, A.J., Paskey, A.C., Kuhn, J.H., Bishop-Lilly, K.A., and Goldberg, T.L. (2020). Diversity, transmission, and cophylogeny of ledanteviruses (Rhabdoviridae: Ledantevirus) and nycteribiid bat flies parasitizing Angolan soft-furred fruit bats in Bundibugyo District, Uganda. Microorganisms, 8.","DOI":"10.3390\/microorganisms8050750"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1089\/vbz.2017.2213","article-title":"Molecular detection of Bartonella species in blood-feeding bat flies from M\u00e9xico","volume":"18","author":"Moskaluk","year":"2018","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1089\/vbz.2017.2163","article-title":"Detection of Dengue virus in bat flies (Diptera: Streblidae) of common vampire bats, Desmodus rotundus, in Progreso, Hidalgo, Mexico","volume":"18","author":"Chomel","year":"2018","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"5287","DOI":"10.1038\/s41598-017-05236-w","article-title":"Kanyawara virus: A novel Rhabdovirus infecting newly discovered nycteribiid bat flies infesting previously unknown pteropodid bats in Uganda","volume":"7","author":"Goldberg","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1038\/s41586-020-2812-9","article-title":"Relatives of rubella virus in diverse mammals","volume":"586","author":"Bennett","year":"2020","journal-title":"Nature"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Bennett, A.J., and Goldberg, T.L. (2020). Pteropine orthoreovirus in an Angolan soft-furred fruit bat (Lissonycteris angolensis) in Uganda dramatically expands the global distribution of an emerging bat-borne respiratory virus. Viruses, 12.","DOI":"10.3390\/v12070740"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1186\/s13071-019-3517-5","article-title":"Surface sterilization methods impact measures of internal microbial diversity in ticks","volume":"12","author":"Binetruy","year":"2019","journal-title":"Parasit. Vectors"},{"key":"ref_21","first-page":"294","article-title":"DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates","volume":"3","author":"Folmer","year":"1994","journal-title":"Mol. Mar. Biol. Biotechnol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic local alignment search tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1007\/978-1-62703-646-7_10","article-title":"Phylogeny-aware alignment with PRANK","volume":"1079","year":"2014","journal-title":"Methods Mol. Biol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1093\/oxfordjournals.molbev.a026334","article-title":"Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis","volume":"17","author":"Castresana","year":"2000","journal-title":"Mol. Biol. Evol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"W7","DOI":"10.1093\/nar\/gkq291","article-title":"TranslatorX: Multiple alignment of nucleotide sequences guided by amino acid translations","volume":"38","author":"Abascal","year":"2010","journal-title":"Nucleic Acids Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1093\/sysbio\/syq010","article-title":"New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0","volume":"59","author":"Guindon","year":"2010","journal-title":"Syst. Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2422","DOI":"10.1093\/molbev\/msx149","article-title":"SMS: Smart model selection in PhyML","volume":"34","author":"Lefort","year":"2017","journal-title":"Mol. Biol. Evol."},{"key":"ref_28","first-page":"64","article-title":"Metagenomic assessment of adventitious viruses in commercial bovine sera","volume":"47","author":"Sibley","year":"2017","journal-title":"Biol. J. Int. Assoc. Biol. Stand."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"20190613","DOI":"10.1098\/rstb.2019.0613","article-title":"Demography, life-history trade-offs, and the gastrointestinal virome of wild chimpanzees","volume":"375","author":"Negrey","year":"2020","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"14498","DOI":"10.1038\/s41598-020-71459-z","article-title":"Mass mortality in freshwater mussels (Actinonaias pectorosa) in the Clinch River, USA, linked to a novel densovirus","volume":"10","author":"Richard","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1186\/1743-422X-10-69","article-title":"Malpais spring virus is a new species in the genus Vesiculovirus","volume":"10","author":"Vasilakis","year":"2013","journal-title":"Virol. J."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"299","DOI":"10.4269\/ajtmh.1977.26.299","article-title":"Isfahan virus, a new vesiculovirus infecting humans, gerbils, and sandflies in Iran","volume":"26","author":"Tesh","year":"1977","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2325","DOI":"10.1007\/s00705-016-2905-9","article-title":"Complete genome sequence of Piry vesiculovirus","volume":"161","author":"Acrani","year":"2016","journal-title":"Arch. Virol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"44","DOI":"10.2174\/1874357901812010044","article-title":"Chandipura viral encephalitis: A brief review","volume":"12","author":"Sapkal","year":"2018","journal-title":"Open Virol. J."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1016\/S0168-1702(02)00026-6","article-title":"Emergence and re-emergence of vesicular stomatitis in the United States","volume":"85","author":"Rodriguez","year":"2002","journal-title":"Virus Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"80","DOI":"10.2174\/1874357901812010080","article-title":"Zoonotic viral diseases of equines and their impact on human and animal health","volume":"12","author":"Kumar","year":"2018","journal-title":"Open Virol. J."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1016\/j.coviro.2018.12.005","article-title":"Bluetongue and epizootic hemorrhagic disease viruses: Recent developments with these globally re-emerging arboviral infections of ruminants","volume":"34","author":"Maclachlan","year":"2019","journal-title":"Curr. Opin. Virol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"21677","DOI":"10.1038\/s41598-020-78673-9","article-title":"Global emergence and evolutionary dynamics of bluetongue virus","volume":"10","author":"Alkhamis","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"353","DOI":"10.20506\/rst.34.2.2362","article-title":"Zoonotic and emerging orbivirus infections","volume":"34","author":"Attoui","year":"2015","journal-title":"Rev. Sci. Tech."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"348","DOI":"10.1089\/vbz.2014.1703","article-title":"Transmission and epidemiology of bluetongue and epizootic hemorrhagic disease in North America: Current perspectives, research gaps, and future directions","volume":"15","author":"Ruder","year":"2015","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1038\/nature20167","article-title":"Redefining the invertebrate RNA virosphere","volume":"540","author":"Shi","year":"2016","journal-title":"Nature"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Evans, A.B., and Peterson, K.E. (2019). Throw out the map: Neuropathogenesis of the globally expanding California serogroup of orthobunyaviruses. Viruses, 11.","DOI":"10.3390\/v11090794"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Edridge, A.W.D., and van der Hoek, L. (2020). Emerging orthobunyaviruses associated with CNS disease. PLoS Negl. Trop. Dis., 14.","DOI":"10.1371\/journal.pntd.0008856"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1099\/jgv.0.001365","article-title":"ICTV virus taxonomy profile: Peribunyaviridae","volume":"101","author":"Hughes","year":"2020","journal-title":"J. Gen. Virol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1016\/0035-9203(74)90069-8","article-title":"Bwamba virus infection: A sero-survey of veterbrates in five ecological zones in Nigeria","volume":"68","author":"Tomori","year":"1974","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1016\/0035-9203(85)90105-1","article-title":"Isolation of Chikungunya and Pongola viruses from patients in Uganda","volume":"79","author":"Kalunda","year":"1985","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1093\/oxfordjournals.aje.a120659","article-title":"The epidemiology of EEE WEE, SLE and turlock viruses, with special reference to birds, in a tropical rain forest near Belem, Brazil","volume":"84","author":"Shope","year":"1966","journal-title":"Am. J. Epidemiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1071\/BI9750425","article-title":"Electron microscopy of Japanaut and Tilligerry viruses: Two proposed members of the orbivirus group","volume":"28","author":"Schnagl","year":"1975","journal-title":"Aust. J. Biol. Sci."},{"key":"ref_49","first-page":"40","article-title":"IFE: A new African orbivirus isolated from Eidolon helvum bats captured in Nigeria, Cameroon and the Central African Republic","volume":"81","author":"Kemp","year":"1987","journal-title":"Bull. Soc. Pathol. Exot. Fil."},{"key":"ref_50","first-page":"180","article-title":"Isolation of the Fom\u00e9d\u00e9 virus from Chiroptera, Nycteris nana, in the Republic of Guinea","volume":"79","author":"Boiro","year":"1985","journal-title":"Bull. Soc. Pathol. Exot. Fil."},{"key":"ref_51","doi-asserted-by":"crossref","unstructured":"Fagre, A.C., Lee, J.S., Kityo, R.M., Bergren, N.A., Mossel, E.C., Nakayiki, T., Nalikka, B., Nyakarahuka, L., Gilbert, A.T., and Peterhans, J.K. (2019). Discovery and characterization of Bukakata orbivirus (Reoviridae:Orbivirus), a novel virus from a Ugandan bat. Viruses, 11.","DOI":"10.3390\/v11030209"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1007\/BF01315626","article-title":"Viruses isolated from bats in Japan","volume":"53","author":"Miura","year":"1977","journal-title":"Arch. Virol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"697","DOI":"10.4269\/ajtmh.1970.19.697","article-title":"Matucare virus, a new agent recovered from Ornithodoros (Alectorobius) boliviensis","volume":"19","author":"Justines","year":"1970","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1654\/4264.1","article-title":"Bolivian ectoparasites: A survey of bats (Mammalia: Chiroptera)","volume":"74","author":"Dick","year":"2007","journal-title":"Comp. Parasitol."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Kunz, T.H., and Parsons, S. (2009). Collecting and preserving ectoparasites for ecological study. Ecological and Behavioral Methods for the Study of Bats, Johns Hopkins University Press. [2nd ed.].","DOI":"10.56021\/9780801891472"},{"key":"ref_56","unstructured":"Mullen, G.R., and Durden, L.A. (2019). Louse Flies, Keds, and Bat Flies (Hippoboscoidea). Medical and Veterinary Entomology, Academic Press. [3rd ed.]."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"2685","DOI":"10.1099\/vir.0.19294-0","article-title":"Isolation of Kaeng Khoi virus from dead Chaerephon plicata bats in Cambodia","volume":"84","author":"Osborne","year":"2003","journal-title":"J. Gen. Virol."},{"key":"ref_58","first-page":"365","article-title":"Kaeng Khoi virus from naturally infected bedbugs (Cimicidae) and immature free-tailed bats","volume":"53","author":"Williams","year":"1976","journal-title":"Bull. World Health Organ."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Groseth, A., Mampilli, V., Weisend, C., Dahlstrom, E., Porcella, S.F., Russell, B.J., Tesh, R.B., and Ebihara, H. (2014). Molecular characterization of human pathogenic bunyaviruses of the Nyando and Bwamba\/Pongola virus groups leads to the genetic identification of Mojui dos Campos and Kaeng Khoi virus. PLoS Negl. Trop. Dis., 8.","DOI":"10.1371\/journal.pntd.0003147"},{"key":"ref_60","unstructured":"Karabatsos, N. (1985). Mojui dos Campos. International Catalogue of Arboviruses Including Certain Other Viruses of Vertebrates, American Society of Tropical Medicine and Hygiene. [3rd ed.]."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1168","DOI":"10.1016\/j.cell.2018.02.043","article-title":"Using metagenomics to characterize an expanding virosphere","volume":"172","author":"Zhang","year":"2018","journal-title":"Cell"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1146\/annurev-virology-092818-015851","article-title":"Expanding the RNA virosphere by unbiased metagenomics","volume":"6","author":"Zhang","year":"2019","journal-title":"Annu. Rev. Virol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"29","DOI":"10.12933\/therya-18-548","article-title":"Bats associated to caves in Jalisco, Mexico","volume":"9","year":"2018","journal-title":"THERYA"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"1740","DOI":"10.1038\/s41598-020-58521-6","article-title":"Between roost contact is essential for maintenance of European bat lyssavirus type-2 in Myotis daubentonii bat reservoir: \u2018The Swarming Hypothesis\u2019","volume":"10","author":"Horton","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1815","DOI":"10.1038\/ismej.2015.247","article-title":"The role of hyperparasitism in microbial pathogen ecology and evolution","volume":"10","author":"Parratt","year":"2016","journal-title":"ISME J."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1016\/j.pt.2018.06.006","article-title":"Bats, bat flies, and fungi: A case of hyperparasitism","volume":"34","author":"Haelewaters","year":"2018","journal-title":"Trends Parasitol."},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Wenzel, R.L., and Tipton, V.J. (1966). Some relationships between mammal hosts and their ectoparasites. Ectoparasites of Panama, Field Museum of Natural History.","DOI":"10.5962\/bhl.title.2633"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1140","DOI":"10.1126\/science.182.4117.1140","article-title":"Transovarial transmission of LaCrosse virus (California encephalitis group) in the mosquito, Aedes triseriatus","volume":"182","author":"Watts","year":"1973","journal-title":"Science"},{"key":"ref_69","doi-asserted-by":"crossref","unstructured":"Rozo-Lopez, P., Drolet, B.S., and Londo\u00f1o-Renteria, B. (2018). Vesicular stomatitis virus transmission: A comparison of incriminated vectors. Insects, 9.","DOI":"10.3390\/insects9040190"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"653","DOI":"10.4269\/ajtmh.1987.36.653","article-title":"Natural infection of humans, animals, and phlebotomine sand flies with the Alagoas serotype of vesicular stomatitis virus in Colombia","volume":"36","author":"Tesh","year":"1987","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"476","DOI":"10.4269\/ajtmh.1990.42.476","article-title":"Isolation of vesicular stomatitis virus New Jersey serotype from phlebotomine sand flies in Georgia","volume":"42","author":"Corn","year":"1990","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1093\/jmedent\/29.2.368","article-title":"Titers of vesicular stomatitis virus, New Jersey serotype, in naturally infected male and female Lutzomyia shannoni (Diptera: Psychodidae) in Georgia","volume":"29","author":"Comer","year":"1992","journal-title":"J. Med. Entomol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"483","DOI":"10.4269\/ajtmh.1990.42.483","article-title":"Vesicular stomatitis virus, New Jersey serotype: Replication in and transmission by Lutzomyia shannoni (Diptera: Psychodidae)","volume":"42","author":"Comer","year":"1990","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1603\/0022-2585-39.4.680","article-title":"Sampling for sand flies (Diptera: Psychodidae) among prairie dog colonies on ranches with histories of vesicular stomatitis in new Mexico and Colorado","volume":"39","author":"Schmidtmann","year":"2002","journal-title":"J. Med. Entomol."},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"Fleming, T.H. (2019). Bat Migration. Encycl. Anim. Behav., 605\u2013610.","DOI":"10.1016\/B978-0-12-809633-8.20764-4"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1890\/ES13-00023.1","article-title":"Moving across the border: Modeling migratory bat populations","volume":"4","author":"Wiederholt","year":"2013","journal-title":"Ecosphere"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"586","DOI":"10.4269\/ajtmh.1988.39.586","article-title":"Malpais spring virus: A new vesiculovirus from mosquitoes collected in New Mexico and evidence of infected indigenous and exotic ungulates","volume":"39","author":"Clark","year":"1988","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"257","DOI":"10.11646\/zootaxa.4560.2.2","article-title":"Vampire in the darkness: A new genus and species of land leech exclusively bloodsucking cave-dwelling bats from China (Hirudinda: Arhynchobdellida: Haemadipsidae)","volume":"4560","author":"Huang","year":"2019","journal-title":"Zootaxa"}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/5\/860\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:58:09Z","timestamp":1760162289000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/13\/5\/860"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,8]]},"references-count":78,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2021,5]]}},"alternative-id":["v13050860"],"URL":"https:\/\/doi.org\/10.3390\/v13050860","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,8]]}}}