{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,3]],"date-time":"2026-10-03T11:08:52Z","timestamp":1791025732822,"version":"4.1.0"},"reference-count":63,"publisher":"Microbiology Society","issue":"10","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2003,10,1]]},"abstract":"<jats:p>Recombination is increasingly seen as an important means of shaping genetic diversity in RNA viruses. However, observed recombination frequencies vary widely among those viruses studied to date, with only sporadic occurrences reported in RNA viruses with negative-sense genomes. To determine the extent of homologous recombination in negative-sense RNA viruses, phylogenetic analyses of 79 gene sequence alignments from 35 negative-sense RNA viruses (a total of 2154 sequences) were carried out. Powerful evidence was found for recombination, in the form of incongruent phylogenetic trees between different gene regions, in only five sequences from <jats:italic>Hantaan virus<\/jats:italic>, <jats:italic>Mumps virus<\/jats:italic> and <jats:italic>Newcastle disease virus<\/jats:italic>. This is the first report of recombination in these viruses. More tentative evidence for recombination, where conflicting phylogenetic trees were observed (but were without strong bootstrap support) and\/or where putative recombinant regions were very short, was found in three alignments from La Crosse virus and <jats:italic>Puumala virus<\/jats:italic>. Finally, patterns of sequence variation compatible with the action of recombination, but not definitive evidence for this process, were observed in a further ten viruses: <jats:italic>Canine distemper virus<\/jats:italic>, <jats:italic>Crimean-Congo haemorrhagic fever virus<\/jats:italic>, <jats:italic>Influenza A<\/jats:italic> \n                  <jats:italic>virus<\/jats:italic>, <jats:italic>Influenza B<\/jats:italic> \n                  <jats:italic>virus<\/jats:italic>, <jats:italic>Influenza C<\/jats:italic> \n                  <jats:italic>virus<\/jats:italic>, <jats:italic>Lassa virus<\/jats:italic>, <jats:italic>Pirital virus<\/jats:italic>, <jats:italic>Rabies virus<\/jats:italic>, <jats:italic>Rift Valley Fever virus<\/jats:italic> and <jats:italic>Vesicular stomatitis virus<\/jats:italic>. The possibility of recombination in these viruses should be investigated further. Overall, this study reveals that rates of homologous recombination in negative-sense RNA viruses are very much lower than those of mutation, with many viruses seemingly clonal on current data. Consequently, recombination rate is unlikely to be a trait that is set by natural selection to create advantageous or purge deleterious mutations.<\/jats:p>","DOI":"10.1099\/vir.0.19277-0","type":"journal-article","created":{"date-parts":[[2003,9,18]],"date-time":"2003-09-18T03:18:12Z","timestamp":1063855092000},"page":"2691-2703","source":"Crossref","is-referenced-by-count":240,"title":["Phylogenetic analysis reveals a low rate of homologous recombination in negative-sense RNA viruses"],"prefix":"10.1099","volume":"84","author":[{"given":"Elizabeth R.","family":"Chare","sequence":"first","affiliation":[{"name":"Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ernest A.","family":"Gould","sequence":"additional","affiliation":[{"name":"Centre for Ecology and Hydrology, Mansfield Road, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edward C.","family":"Holmes","sequence":"additional","affiliation":[{"name":"Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"345","reference":[{"key":"R1","doi-asserted-by":"crossref","first-page":"1339","DOI":"10.1099\/0022-1317-80-6-1339","article-title":"Recombination in RNA viruses and in virus-resistant transgenic plants","volume":"80","author":"Aaziz","year":"1999","journal-title":"J Gen Virol"},{"key":"R2","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1006\/viro.2002.1695","article-title":"High genetic divergence and recombination in arenaviruses from the Americas","volume":"304","author":"Archer","year":"2002","journal-title":"Virology"},{"key":"R3","doi-asserted-by":"crossref","first-page":"2833","DOI":"10.1099\/0022-1317-81-12-2833","article-title":"Molecular evolution of puumala hantavirus in Fennoscandia: phylogenetic analysis of strains from two recolonization routes","volume":"81","author":"Asikainen","year":"2000","journal-title":"Karelia and Denmark. J Gen Virol"},{"key":"R4","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1006\/smvy.1997.0108","article-title":"Nodavirus RNA recombination","volume":"8","author":"Ball","year":"1997","journal-title":"Semin Virol"},{"key":"R5","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1016\/0042-6822(91)90795-D","article-title":"Random nature of coronavirus RNA recombination in the absence of selection pressure","volume":"185","author":"Banner","year":"1991","journal-title":"Virology"},{"key":"R6","doi-asserted-by":"crossref","first-page":"1577","DOI":"10.1098\/rspb.1996.0231","article-title":"Viral quasi-species and recombination","volume":"263","author":"Boerlijst","year":"1996","journal-title":"Proc R Soc Lond B Biol Sci"},{"key":"R7","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1006\/smvy.1996.0044","article-title":"Different mechanisms of homologous and nonhomologous recombination in brome mosaic virus: role of RNA sequences and replicase proteins","volume":"7","author":"Bujarski","year":"1996","journal-title":"Semin Virol"},{"key":"R8","doi-asserted-by":"crossref","first-page":"253","DOI":"10.3201\/eid0303.970301","article-title":"Recombination in HIV: an important viral evolutionary strategy","volume":"3","author":"Burke","year":"1997","journal-title":"Emerg Infect Dis"},{"key":"R9","doi-asserted-by":"crossref","first-page":"4822","DOI":"10.1128\/JVI.67.8.4822-4830.1993","article-title":"The rule of six, a basic feature for efficient replication of Sendai virus defective interfering RNA","volume":"67","author":"Calain","year":"1993","journal-title":"J Virol"},{"key":"R10","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1006\/viro.1999.9915","article-title":"Ebola virus defective interfering particles and persistent infection","volume":"262","author":"Calain","year":"1999","journal-title":"Virology"},{"key":"R11","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1038\/348454a0","article-title":"Fitness of RNA virus decreased by Muller's ratchet","volume":"348","author":"Chao","year":"1990","journal-title":"Nature"},{"key":"R12","first-page":"233","article-title":"Evolution of genetic exchange in RNA viruses","volume-title":"In The Evolutionary Biology of Viruses","author":"Chao","year":"1994"},{"key":"R13","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1006\/viro.2001.0874","article-title":"The Whitewater Arroyo virus: natural evidence for genetic recombination among Tacaribe serocomplex viruses (family Arenaviridae","volume":"283","author":"Charrel","year":"2001","journal-title":"Virology"},{"key":"R14","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1006\/smvy.1997.0113","article-title":"Recombination in bacteriophage Q \u03b2 its satellite RNAs: the in vivo and in vitro studies","volume":"8","author":"Chetverin","year":"1997","journal-title":"Semin Virol"},{"key":"R15","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1146\/annurev.genet.32.1.123","article-title":"Nonsegmented negative-strand RNA viruses: genetics and manipulation of viral genomes","volume":"32","author":"Conzelmann","year":"1998","journal-title":"Annu Rev Genet"},{"key":"R16","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1099\/0022-1317-23-1-41","article-title":"On the nature of poliovirus genetic recombinants","volume":"23","author":"Cooper","year":"1974","journal-title":"J Gen Virol"},{"key":"R17","doi-asserted-by":"crossref","first-page":"6895","DOI":"10.1073\/pnas.111085598","article-title":"RNA virus error catastrophe: direct molecular test by using ribavirin","volume":"98","author":"Crotty","year":"2001","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R18","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1016\/0168-1702(93)90037-N","article-title":"Establishment of persistent reovirus infection in SC1 cells: absence of protein synthesis inhibition and increased level of double-stranded RNA-activated protein kinase","volume":"27","author":"Danis","year":"1993","journal-title":"Virus Res"},{"key":"R19","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1146\/annurev.micro.51.1.151","article-title":"RNA virus mutations for fitness and survival","volume":"51","author":"Domingo","year":"1997","journal-title":"Annu Rev Microbiol"},{"key":"R20","doi-asserted-by":"crossref","first-page":"13910","DOI":"10.1073\/pnas.96.24.13910","article-title":"Mutation rates among RNA viruses","volume":"96","author":"Drake","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R21","doi-asserted-by":"crossref","first-page":"6015","DOI":"10.1073\/pnas.89.13.6015","article-title":"Rapid fitness losses in mammalian RNA virus clones due to Muller's ratchet","volume":"89","author":"Duarte","year":"1992","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R22","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1006\/viro.1998.9267","article-title":"Heterologous protection of mice from a lethal human H1N1 influenza A virus infection by H3N8 equine defective interfering virus: comparison of defective RNA sequences isolated from the DI inoculum and mouse lung","volume":"248","author":"Duhaut","year":"1998","journal-title":"Virology"},{"key":"R23","doi-asserted-by":"crossref","first-page":"2233","DOI":"10.1128\/JVI.63.5.2233-2243.1989","article-title":"The Sendai virus nucleocapsid exists in at least four different helical states","volume":"63","author":"Egelman","year":"1989","journal-title":"J Virol"},{"key":"R24","doi-asserted-by":"crossref","first-page":"1078","DOI":"10.1046\/j.1420-9101.1999.00110.x","article-title":"Rate of deleterious mutation and the distribution of its effects on fitness in vesicular stomatitis virus","volume":"12","author":"Elena","year":"1999","journal-title":"J Evol Biol"},{"key":"R25","doi-asserted-by":"crossref","first-page":"1842","DOI":"10.1126\/science.1061662","article-title":"Recombination in the hemagglutinin gene of the 1918 \u2018Spanish flu\u2019","volume":"293","author":"Gibbs","year":"2001","journal-title":"Science"},{"key":"R26","first-page":"75","article-title":"Evolutionary processes in influenza viruses: divergence, rapid evolution, and stasis","volume":"176","author":"Gorman","year":"1992","journal-title":"Curr Top Microbiol Immunol"},{"key":"R27","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1111\/j.1348-0421.1992.tb01663.x","article-title":"Molecular analysis of virus-producing and non-producing clones derived from a defective SSPE virus Yamagata-1 strain","volume":"36","author":"Haga","year":"1992","journal-title":"Microbiol Immunol"},{"key":"R28","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1093\/oxfordjournals.molbev.a026121","article-title":"Phylogenetic evidence for recombination in dengue virus","volume":"16","author":"Holmes","year":"1999","journal-title":"Mol Biol Evol"},{"key":"R29","doi-asserted-by":"crossref","first-page":"1227","DOI":"10.1126\/science.1700865","article-title":"Retroviral recombination and reverse transcription","volume":"250","author":"Hu","year":"1990","journal-title":"Science"},{"key":"R30","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1007\/s00239-001-0064-3","article-title":"Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis","volume":"54","author":"Jenkins","year":"2002","journal-title":"J Mol Evol"},{"key":"R31","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1016\/0092-8674(83)90394-X","article-title":"Does the higher order structure of the influenza virus ribonucleoprotein guide sequence rearrangements in influenza viral RNA?","volume":"34","author":"Jennings","year":"1983","journal-title":"Cell"},{"key":"R32","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1038\/418144a","article-title":"Multiply infected spleen cells in HIV patients","volume":"418","author":"Jung","year":"2002","journal-title":"Nature"},{"key":"R33","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1007\/s007050050527","article-title":"Sequence analysis of F, SH, and HN genes among mumps virus strains in Japan","volume":"144","author":"Kashiwagi","year":"1999","journal-title":"Arch Virol"},{"key":"R34","doi-asserted-by":"crossref","first-page":"804","DOI":"10.1128\/JVI.77.1.804-809.2003","article-title":"Genetic interaction between distinct Dobrava hantavirus subtypes in Apodemus agrarius and A. flavicollis in nature","volume":"77","author":"Klempa","year":"2003","journal-title":"J Virol"},{"key":"R35","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1128\/JVI.72.2.891-899.1998","article-title":"Paramyxovirus RNA synthesis and the requirement for hexamer genome length: the rule of six revisited","volume":"72","author":"Kolakofsky","year":"1998","journal-title":"J Virol"},{"key":"R36","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1128\/MMBR.56.1.61-79.1992","article-title":"RNA recombination in animal and plant viruses","volume":"56","author":"Lai","year":"1992","journal-title":"Microbiol Rev"},{"key":"R37","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1006\/viro.1997.8571","article-title":"Replication signals in the genome of the vesicular stomatitis virus and its defective interfering particles: identification of a sequence element that enhances DI RNA replication","volume":"232","author":"Li","year":"1997","journal-title":"Virology"},{"key":"R38","doi-asserted-by":"crossref","first-page":"6117","DOI":"10.1128\/JVI.66.10.6117-6124.1992","article-title":"RNA recombination in a coronavirus: recombination between viral genomic RNA and transfected RNA fragments","volume":"66","author":"Liao","year":"1992","journal-title":"J Virol"},{"key":"R39","doi-asserted-by":"crossref","first-page":"1492","DOI":"10.1073\/pnas.96.4.1492","article-title":"Lethal mutagenesis of HIV with mutagenic nucleoside analogs","volume":"96","author":"Loeb","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R40","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1006\/smvy.1996.0047","article-title":"Heterologous recombination in the segmented dsRNA genome of bacteriophage \u03d5 6","volume":"7","author":"Mindich","year":"1996","journal-title":"Semin Virol"},{"key":"R41","doi-asserted-by":"crossref","first-page":"6106","DOI":"10.1073\/pnas.93.12.6106","article-title":"Recombination leads to the rapid emergence of HIV-1 dually resistant mutants under selective drug pressure","volume":"93","author":"Moutouh","year":"1996","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R42","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1006\/viro.1997.8530","article-title":"Genome nucleotide lengths that are divisible by six are not essential but enhance replication of defective interfering RNAs of the paramyxovirus simian virus 5","volume":"232","author":"Murphy","year":"1997","journal-title":"Virology"},{"key":"R43","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1006\/viro.1994.1555","article-title":"Nonhomologous recombination between the hemagglutinin gene and the nucleoprotein gene of an influenza virus","volume":"204","author":"Orlich","year":"1994","journal-title":"Virology"},{"key":"R44","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1146\/annurev.genet.36.040202.111115","article-title":"Recombination in evolutionary genomics","volume":"36","author":"Posada","year":"2002","journal-title":"Annu Rev Genet"},{"key":"R45","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1099\/0022-1317-59-1-207","article-title":"Measurement of surface antigen by specific bacterial adherence and scanning electron microscopy (SABA\/SEM) in cells infected by vesiculovirus ts mutants","volume":"59","author":"Pringle","year":"1982","journal-title":"J Gen Virol"},{"key":"R46","first-page":"235","article-title":"seq-gen: an application for the Monte Carlo simulation of DNA sequence evolution along phylogenetic trees","volume":"13","author":"Rambaut","year":"1997","journal-title":"Comput Appl Biosci"},{"key":"R47","doi-asserted-by":"crossref","first-page":"124","DOI":"10.1038\/374124b0","article-title":"Recombination in HIV-1","volume":"374","author":"Robertson","year":"1995","journal-title":"Nature"},{"key":"R48","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1146\/annurev.phyto.35.1.191","article-title":"Mechanisms of plant virus evolution","volume":"35","author":"Roossinck","year":"1997","journal-title":"Annu Rev Phytopathol"},{"key":"R49","first-page":"526","article-title":"Statistical tests for detecting gene conversion","volume":"6","author":"Sawyer","year":"1989","journal-title":"Mol Biol Evol"},{"key":"R50","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1016\/S0168-1702(01)00427-0","article-title":"Nucleotide sequence analysis of the Newcastle disease virus nucleocapsid protein gene and phylogenetic relationships among the Paramyxoviridae","volume":"83","author":"Seal","year":"2002","journal-title":"Virus Res"},{"key":"R51","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1128\/JVI.73.1.667-675.1999","article-title":"Recombination in Tula hantavirus evolution: analysis of genetic lineages from Slovakia","volume":"73","author":"Sibold","year":"1999","journal-title":"J Virol"},{"key":"R52","doi-asserted-by":"crossref","first-page":"8316","DOI":"10.1128\/JVI.74.18.8316-8323.2000","article-title":"Response of foot-and-mouth disease virus to increased mutagenesis: influence of viral load and fitness in loss of infectivity","volume":"74","author":"Sierra","year":"2000","journal-title":"J Virol"},{"key":"R53","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1146\/annurev.py.32.090194.002005","article-title":"RNA\u2013RNA recombination and evolution in virus-infected plants","volume":"32","author":"Simon","year":"1994","journal-title":"Annu Rev Phytopath"},{"key":"R54","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/0042-6822(90)90494-C","article-title":"Cellular mechanisms in the superinfection exclusion of vesicular stomatitis virus","volume":"177","author":"Simon","year":"1990","journal-title":"Virology"},{"key":"R55","doi-asserted-by":"crossref","first-page":"11803","DOI":"10.1128\/JVI.75.23.11803-11810.2001","article-title":"Molecular evolution of Puumala hantavirus","volume":"75","author":"Sironen","year":"2001","journal-title":"J Virol"},{"key":"R56","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1006\/smvy.1997.0115","article-title":"Recombination in alphaviruses","volume":"8","author":"Strauss","year":"1997","journal-title":"Semin Virol"},{"key":"R57","volume-title":"paup*: Phylogenetic Analysis Using Parsimony (*and Other Methods), version 4","author":"Swofford","year":"2002"},{"key":"R58","doi-asserted-by":"crossref","first-page":"4876","DOI":"10.1093\/nar\/25.24.4876","article-title":"The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools","volume":"25","author":"Thompson","year":"1997","journal-title":"Nucleic Acids Res"},{"key":"R59","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1099\/0022-1317-73-4-829","article-title":"Cloning and sequencing of Puumala virus Sotkamo strain S and M RNA segments: evidence for strain variation in hantaviruses and expression of the nucleocapsid protein","volume":"73","author":"Vapalahti","year":"1992","journal-title":"J Gen Virol"},{"key":"R60","doi-asserted-by":"crossref","first-page":"1425","DOI":"10.1093\/oxfordjournals.molbev.a003928","article-title":"A novel approach to detecting and measuring recombination: new insights into evolution in viruses, bacteria, and mitochondria","volume":"18","author":"Worobey","year":"2001","journal-title":"Mol Biol Evol"},{"key":"R61","doi-asserted-by":"crossref","first-page":"2535","DOI":"10.1099\/0022-1317-80-10-2535","article-title":"Evolutionary aspects of recombination in RNA viruses","volume":"80","author":"Worobey","year":"1999","journal-title":"J Gen Virol"},{"key":"R62","doi-asserted-by":"crossref","first-page":"7352","DOI":"10.1073\/pnas.96.13.7352","article-title":"Widespread intra-serotype recombination in natural populations of dengue virus","volume":"96","author":"Worobey","year":"1999","journal-title":"Proc Natl Acad Sci U S A"},{"key":"R63","doi-asserted-by":"crossref","first-page":"211","DOI":"10.1126\/science.296.5566.211a","article-title":"Questioning the evidence for genetic recombination in the 1918 \u2018Spanish flu\u2019 virus","volume":"296","author":"Worobey","year":"2002","journal-title":"Science"}],"container-title":["Journal of General Virology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/jgv\/10.1099\/vir.0.19277-0?crawler=true","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,10,6]],"date-time":"2020-10-06T13:24:28Z","timestamp":1601990668000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.microbiologyresearch.org\/content\/journal\/jgv\/10.1099\/vir.0.19277-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,10,1]]},"references-count":63,"journal-issue":{"issue":"10","published-print":{"date-parts":[[2003,10,1]]}},"URL":"https:\/\/doi.org\/10.1099\/vir.0.19277-0","relation":{},"ISSN":["0022-1317","1465-2099"],"issn-type":[{"value":"0022-1317","type":"print"},{"value":"1465-2099","type":"electronic"}],"subject":[],"published":{"date-parts":[[2003,10,1]]}}}