{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,22]],"date-time":"2026-03-22T01:19:01Z","timestamp":1774142341998,"version":"3.50.1"},"reference-count":56,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,10,19]],"date-time":"2017-10-19T00:00:00Z","timestamp":1508371200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,10,19]],"date-time":"2017-10-19T00:00:00Z","timestamp":1508371200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Rabbit hemorrhagic disease (RHD) is a veterinary disease that affects the European rabbit and has a significant economic and ecological negative impact. In Portugal, rabbit hemorrhagic disease virus (RHDV) was reported in 1989 and still causes enzootic outbreaks. Several recombination events have been detected in RHDV strains, including in the first reported outbreak. Here we describe the occurrence of recombination in RHDV strains recovered from rabbit and Iberian hare samples collected in the mid-1990s in Portugal. Characterization of full genomic sequences revealed the existence of a single recombination breakpoint at the boundary of the non-structural and the structural encoding regions, further supporting the importance of this region as a recombination hotspot in lagoviruses. Phylogenetic analysis showed that in the structural region, the recombinant strains were similar to pathogenic G1 strains, but in the non-structural region they formed a new group that diverged ~13% from known strains. No further reports of such group exist, but this recombination event was also detected in an Iberian hare that was associated with the earliest species jump in RHDV. Our results highlight the importance of the characterization of full genomes to disclose RHDV evolution and show that lagoviruses\u2019 diversity has been significantly undersampled.<\/jats:p>","DOI":"10.1038\/s41598-017-13902-2","type":"journal-article","created":{"date-parts":[[2017,10,13]],"date-time":"2017-10-13T14:53:03Z","timestamp":1507906383000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Characterization of old RHDV strains by complete genome sequencing identifies a novel genetic group"],"prefix":"10.1038","volume":"7","author":[{"given":"Ana M.","family":"Lopes","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2254-1230","authenticated-orcid":false,"given":"Diogo","family":"Silv\u00e9rio","sequence":"additional","affiliation":[]},{"given":"Maria J.","family":"Magalh\u00e3es","sequence":"additional","affiliation":[]},{"given":"Helena","family":"Areal","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4797-0939","authenticated-orcid":false,"given":"Paulo C.","family":"Alves","sequence":"additional","affiliation":[]},{"given":"Pedro J.","family":"Esteves","sequence":"additional","affiliation":[]},{"given":"Joana","family":"Abrantes","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2017,10,19]]},"reference":[{"key":"13902_CR1","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1111\/j.1365-2907.2009.00140.x","volume":"39","author":"M Delibes-Mateos","year":"2009","unstructured":"Delibes-Mateos, M., Ferreras, P. & Villafuerte, R. European rabbit population trends and associated factors: a review of the situation in the Iberian Peninsula. Mammal Rev \n                           39, 124\u2013140, https:\/\/doi.org\/10.1111\/j.1365-2907.2009.00140 (2009).","journal-title":"Mammal Rev"},{"key":"13902_CR2","first-page":"253","volume":"16","author":"SJ Liu","year":"1984","unstructured":"Liu, S. J., Xue, H. P., Pu, B. Q. & Qian, N. H. A new viral disease in rabbit. Anim Husb Vet Med \n                           16, 253\u2013255 (1984).","journal-title":"Anim Husb Vet Med"},{"key":"13902_CR3","doi-asserted-by":"publisher","DOI":"10.1186\/1297-9716-43-12","volume":"43","author":"J Abrantes","year":"2012","unstructured":"Abrantes, J., van der Loo, W., Le Pendu, J. & Esteves, P. J. Rabbit haemorrhagic disease (RHD) and rabbit haemorrhagic disease virus (RHDV): a review. Vet Res \n                           43, 12, https:\/\/doi.org\/10.1186\/1297-9716-43-12 (2012).","journal-title":"Vet Res"},{"key":"13902_CR4","unstructured":"Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. (Elsevier, 2012)."},{"key":"13902_CR5","doi-asserted-by":"publisher","first-page":"664","DOI":"10.1016\/0042-6822(91)90436-F","volume":"184","author":"G Meyers","year":"1991","unstructured":"Meyers, G., Wirblich, C. & Thiel, H. J. Rabbit hemorrhagic disease virus-molecular cloning and nucleotide sequencing of a calicivirus genome. Virology \n                           184, 664\u2013676, https:\/\/doi.org\/10.1016\/0042-6822(91)90436-F (1991).","journal-title":"Virology"},{"key":"13902_CR6","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1006\/viro.2000.0545","volume":"276","author":"G Meyers","year":"2000","unstructured":"Meyers, G., Wirblich, C., Thiel, H. J. & Thumfart, J. O. Rabbit hemorrhagic disease virus: genome organization and polyprotein processing of a calicivirus studied after transient expression of cDNA constructs. Virology \n                           276, 349\u2013363, https:\/\/doi.org\/10.1006\/viro.2000.0545 (2000).","journal-title":"Virology"},{"key":"13902_CR7","doi-asserted-by":"publisher","first-page":"677","DOI":"10.1016\/0042-6822(91)90437-G","volume":"184","author":"G Meyers","year":"1991","unstructured":"Meyers, G., Wirblich, C. & Thiel, H.-J. Genomic and subgenomic RNAs of rabbit hemorrhagic disease virus are both protein-linked and packaged into particles. Virology \n                           184, 677\u2013686, https:\/\/doi.org\/10.1016\/0042-6822(91)90437-G (1991).","journal-title":"Virology"},{"key":"13902_CR8","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1005087","volume":"11","author":"PJ Esteves","year":"2015","unstructured":"Esteves, P. J. et al. Emergence of Pathogenicity in Lagoviruses: Evolution from Pre-existing Nonpathogenic Strains or through a Species Jump? PLoS Pathog \n                           11, e1005087, https:\/\/doi.org\/10.1371\/journal.ppat.1005087 (2015).","journal-title":"PLoS Pathog"},{"key":"13902_CR9","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1017\/S0950268899003994","volume":"124","author":"BD Cooke","year":"2000","unstructured":"Cooke, B. D., Robinson, A. J., Merchant, J. C., Nardin, A. & Capucci, L. Use of ELISAs in field studies of rabbit haemorrhagic disease (RHD) in Australia. Epidemiol Infect \n                           124, 563\u2013576, https:\/\/doi.org\/10.1017\/S0950268899003994 (2000).","journal-title":"Epidemiol Infect"},{"key":"13902_CR10","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/S0378-1135(98)00307-1","volume":"66","author":"JS O\u2019Keefe","year":"1999","unstructured":"O\u2019Keefe, J. S., Tempero, J. E., Motha, M. X., Hansen, M. F. & Atkinsona, P. H. Serology of rabbit haemorrhagic disease virus in wild rabbits before and after release of the virus in New Zealand. Vet Microbiol \n                           66, 29\u201340, https:\/\/doi.org\/10.1016\/S0378-1135(98)00307-1 (1999).","journal-title":"Vet Microbiol"},{"key":"13902_CR11","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1071\/WR00096","volume":"29","author":"AJ Robinson","year":"2002","unstructured":"Robinson, A. J. et al. Serological evidence for the presence of a calicivirus in Australian wild rabbits, Oryctolagus cuniculus, before the introduction of rabbit haemorrhagic disease virus (RHDV): its potential influence on the specificity of a competitive ELISA for RHDV. Wildl Res \n                           29, 655\u2013662, https:\/\/doi.org\/10.1071\/WR00096 (2002).","journal-title":"Wildl Res"},{"key":"13902_CR12","doi-asserted-by":"publisher","first-page":"1075","DOI":"10.1099\/0022-1317-71-5-1075","volume":"71","author":"L Rodak","year":"1990","unstructured":"Rodak, L. et al. Enzyme-linked immunosorbent assay of antibodies to rabbit haemorrhagic disease virus and determination of its major structural proteins. J Gen Virol \n                           71, 1075\u20131080, https:\/\/doi.org\/10.1099\/0022-1317-71-5-1075 (1990).","journal-title":"J Gen Virol"},{"key":"13902_CR13","doi-asserted-by":"publisher","first-page":"749","DOI":"10.1007\/s007050050668","volume":"145","author":"HS Nagesha","year":"2000","unstructured":"Nagesha, H. S. et al. The presence of cross-reactive antibodies to rabbit haemorrhagic disease virus in Australian wild rabbits prior to the escape of virus from quarantine. Arch Virol \n                           145, 749\u2013757, https:\/\/doi.org\/10.1007\/s007050050668 (2000).","journal-title":"Arch Virol"},{"key":"13902_CR14","doi-asserted-by":"crossref","first-page":"8614","DOI":"10.1128\/jvi.70.12.8614-8623.1996","volume":"70","author":"L Capucci","year":"1996","unstructured":"Capucci, L., Fusi, P., Lavazza, A., Pacciarini, M. L. & Rossi, C. Detection and preliminary characterization of a new rabbit calicivirus related to rabbit hemorrhagic disease virus but nonpathogenic. J Virol \n                           70, 8614\u20138623 (1996).","journal-title":"J Virol"},{"key":"13902_CR15","doi-asserted-by":"publisher","first-page":"42","DOI":"10.1016\/j.virol.2009.07.008","volume":"393","author":"NL Forrester","year":"2009","unstructured":"Forrester, N. L., Boag, B., Buckley, A., Moureau, G. & Gould, E. A. Co-circulation of widely disparate strains of rabbit haemorrhagic disease virus could explain localised epidemicity in the United Kingdom. Virology \n                           393, 42\u201348, https:\/\/doi.org\/10.1016\/j.virol.2009.07.008 (2009).","journal-title":"Virology"},{"key":"13902_CR16","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.virol.2006.09.011","volume":"358","author":"NL Forrester","year":"2007","unstructured":"Forrester, N. L., Trout, R. C. & Gould, E. A. Benign circulation of rabbit haemorrhagic disease virus on Lambay Island, Eire. Virology \n                           358, 18\u201322, https:\/\/doi.org\/10.1016\/j.virol.2006.09.011 (2007).","journal-title":"Virology"},{"key":"13902_CR17","doi-asserted-by":"publisher","first-page":"97","DOI":"10.1016\/j.virol.2008.11.004","volume":"384","author":"T Strive","year":"2009","unstructured":"Strive, T., Wright, J. D. & Robinson, A. J. Identification and partial characterisation of a new Lagovirus in Australian wild rabbits. Virology \n                           384, 97\u2013105, https:\/\/doi.org\/10.1016\/j.virol.2008.11.004 (2009).","journal-title":"Virology"},{"key":"13902_CR18","doi-asserted-by":"publisher","first-page":"1955","DOI":"10.3201\/eid1512.090839","volume":"15","author":"IL Bergin","year":"2009","unstructured":"Bergin, I. L. et al. Novel calicivirus identified in rabbits, Michigan, USA. Emerg Infect Dis \n                           15, 1955\u20131962, https:\/\/doi.org\/10.3201\/eid1512.090839 (2009).","journal-title":"Emerg Infect Dis"},{"key":"13902_CR19","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1016\/j.virol.2010.12.001","volume":"410","author":"G Le Gall-Recul\u00e9","year":"2011","unstructured":"Le Gall-Recul\u00e9, G. et al. Characterisation of a non-pathogenic and non-protective infectious rabbit lagovirus related to RHDV. 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Vet Rec \n                           168, 137\u2013138, https:\/\/doi.org\/10.1136\/vr.d697 (2011).","journal-title":"Vet Rec"},{"key":"13902_CR24","doi-asserted-by":"publisher","first-page":"2009","DOI":"10.3201\/eid1812.120341","volume":"18","author":"KP Dalton","year":"2012","unstructured":"Dalton, K. P. et al. Variant rabbit hemorrhagic disease virus in young rabbits, Spain. Emerg Infect Dis \n                           18, 2009\u20132012, https:\/\/doi.org\/10.3201\/eid1812.120341 (2012).","journal-title":"Emerg Infect Dis"},{"key":"13902_CR25","doi-asserted-by":"publisher","DOI":"10.1186\/1297-9716-44-81","volume":"44","author":"G Le Gall-Recul\u00e9","year":"2013","unstructured":"Le Gall-Recul\u00e9, G. et al. Emergence of a new lagovirus related to Rabbit Haemorrhagic Disease Virus. Vet Res \n                           44, 81, https:\/\/doi.org\/10.1186\/1297-9716-44-81 (2013).","journal-title":"Vet Res"},{"key":"13902_CR26","doi-asserted-by":"publisher","first-page":"642","DOI":"10.1016\/j.rvsc.2014.10.008","volume":"97","author":"A Camarda","year":"2014","unstructured":"Camarda, A. et al. Detection of the new emerging rabbit haemorrhagic disease type 2 virus (RHDV2) in Sicily from rabbit (Oryctolagus cuniculus) and Italian hare (Lepus corsicanus). Res Vet Sci \n                           97, 642\u2013645, https:\/\/doi.org\/10.1016\/j.rvsc.2014.10.008 (2014).","journal-title":"Res Vet Sci"},{"key":"13902_CR27","doi-asserted-by":"publisher","DOI":"10.1186\/1297-9716-44-96","volume":"44","author":"G Puggioni","year":"2013","unstructured":"Puggioni, G. et al. The new French 2010 Rabbit Hemorrhagic Disease Virus causes an RHD-like disease in the Sardinian Cape hare (Lepus capensis mediterraneus). Vet Res \n                           44, 96, https:\/\/doi.org\/10.1186\/1297-9716-44-96 (2013).","journal-title":"Vet Res"},{"key":"13902_CR28","doi-asserted-by":"publisher","unstructured":"Velarde, R. et al. Spillover Events of Infection of Brown Hares (Lepus europaeus) with Rabbit Haemorrhagic Disease Type 2 Virus (RHDV2) Caused Sporadic Cases of an European Brown Hare Syndrome-Like Disease in Italy and Spain. Transboundary and Emerging Diseases, https:\/\/doi.org\/10.1111\/tbed.12562 (2016).","DOI":"10.1111\/tbed.12562"},{"key":"13902_CR29","doi-asserted-by":"publisher","first-page":"1900","DOI":"10.3201\/eid1911.130908","volume":"19","author":"J Abrantes","year":"2013","unstructured":"Abrantes, J. et al. New variant of rabbit hemorrhagic disease virus, Portugal, 2012\u20132013. Emerg Infect Dis \n                           19, 1900\u20131902, https:\/\/doi.org\/10.3201\/eid1911.130908 (2013).","journal-title":"Emerg Infect Dis"},{"key":"13902_CR30","first-page":"645","volume":"5","author":"JL Arg\u00fcello","year":"1988","unstructured":"Arg\u00fcello, J. L., Llanos, A. & P\u00e9rez, L. I. Enfermedad hemorr\u00e1gica del conejo en Espa\u00f1a. Medicina Veterinaria \n                           5, 645\u2013650 (1988).","journal-title":"Medicina Veterinaria"},{"key":"13902_CR31","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2148-10-347","volume":"10","author":"F Alda","year":"2010","unstructured":"Alda, F. et al. Evolutionary history and molecular epidemiology of rabbit haemorrhagic disease virus in the Iberian Peninsula and Western Europe. BMC Evolutionary Biology \n                           10, 347, https:\/\/doi.org\/10.1186\/1471-2148-10-347 (2010).","journal-title":"BMC evolutionary biology"},{"key":"13902_CR32","doi-asserted-by":"publisher","first-page":"368","DOI":"10.1016\/j.vetmic.2008.09.057","volume":"135","author":"A Muller","year":"2009","unstructured":"Muller, A. et al. Evolution of rabbit haemorrhagic disease virus (RHDV) in the European rabbit (Oryctolagus cuniculus) from the Iberian Peninsula. Vet Microbiol \n                           135, 368\u2013373, https:\/\/doi.org\/10.1016\/j.vetmic.2008.09.057 (2009).","journal-title":"Vet Microbiol"},{"key":"13902_CR33","doi-asserted-by":"publisher","first-page":"27","DOI":"10.3390\/v7010027","volume":"7","author":"AM Lopes","year":"2015","unstructured":"Lopes, A. M. et al. Is the New Variant RHDV Replacing Genogroup in Portuguese Wild Rabbit Populations? Viruses \n                           7, 27\u201336, https:\/\/doi.org\/10.3390\/v7010027 (2015).","journal-title":"Viruses"},{"key":"13902_CR34","doi-asserted-by":"publisher","DOI":"10.4995\/wrs.2014.1715","volume":"22","author":"C Calvete","year":"2014","unstructured":"Calvete, C., Sarto, P., Calvo, A. J., Monroy, F. & Calvo, J. H. Could the new rabbit haemorrhagic disease virus variant (RHDVb) be fully replacing classical RHD strains in the Iberian Peninsula? World Rabbit Science \n                           22, 91, https:\/\/doi.org\/10.4995\/wrs.2014.1715 (2014).","journal-title":"World Rabbit Science"},{"key":"13902_CR35","doi-asserted-by":"publisher","first-page":"12129","DOI":"10.1128\/JVI.01523-09","volume":"83","author":"PJ Kerr","year":"2009","unstructured":"Kerr, P. J., Kitchen, A. & Holmes, E. C. Origin and phylodynamics of rabbit hemorrhagic disease virus. J Virol \n                           83, 12129\u201312138, https:\/\/doi.org\/10.1128\/JVI.01523-09 (2009).","journal-title":"J Virol"},{"key":"13902_CR36","doi-asserted-by":"publisher","first-page":"174","DOI":"10.1099\/vir.0.014076-0","volume":"91","author":"M Kinnear","year":"2010","unstructured":"Kinnear, M. & Linde, C. C. Capsid gene divergence in rabbit hemorrhagic disease virus. J Gen Virol \n                           91, 174\u2013181, https:\/\/doi.org\/10.1099\/vir.0.014076-0 (2010).","journal-title":"J Gen Virol"},{"key":"13902_CR37","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2148-12-74","volume":"12","author":"AL Hicks","year":"2012","unstructured":"Hicks, A. L. & Duffy, S. One misdated sequence of rabbit hemorrhagic disease virus prevents accurate estimation of its nucleotide substitution rate. BMC Evolutionary Biology \n                           12, 74, https:\/\/doi.org\/10.1186\/1471-2148-12-74 (2012).","journal-title":"BMC evolutionary biology"},{"key":"13902_CR38","doi-asserted-by":"publisher","first-page":"12217","DOI":"10.1128\/JVI.01937-15","volume":"89","author":"JS Eden","year":"2015","unstructured":"Eden, J. S., Read, A. J., Duckworth, J. A., Strive, T. & Holmes, E. C. Resolving the Origin of Rabbit Hemorrhagic Disease Virus: Insights from an Investigation of the Viral Stocks Released in Australia. J Virol \n                           89, 12217\u201312220, https:\/\/doi.org\/10.1128\/JVI.01937-15 (2015).","journal-title":"J Virol"},{"key":"13902_CR39","doi-asserted-by":"publisher","first-page":"9548","DOI":"10.1128\/JVI.01100-15","volume":"89","author":"JS Eden","year":"2015","unstructured":"Eden, J. S. et al. Comparative Phylodynamics of Rabbit Hemorrhagic Disease Virus in Australia and New Zealand. J Virol \n                           89, 9548\u20139558, https:\/\/doi.org\/10.1128\/JVI.01100-15 (2015).","journal-title":"J Virol"},{"key":"13902_CR40","doi-asserted-by":"publisher","first-page":"1309","DOI":"10.1099\/vir.0.000070","volume":"96","author":"AM Lopes","year":"2015","unstructured":"Lopes, A. M. et al. Full genomic analysis of new variant Rabbit Hemorrhagic Disease Virus revealed multiple recombination events. J Gen Virol \n                           96, 1309\u20131319, https:\/\/doi.org\/10.1099\/vir.0.000070 (2015).","journal-title":"J Gen Virol"},{"key":"13902_CR41","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1007\/s00705-007-1084-0","volume":"153","author":"J Abrantes","year":"2008","unstructured":"Abrantes, J., Esteves, P. J. & van der Loo, W. Evidence for recombination in the major capsid gene VP60 of the rabbit haemorrhagic disease virus (RHDV). Arch Virol \n                           153, 329\u2013335, https:\/\/doi.org\/10.1007\/s00705-007-1084-0 (2008).","journal-title":"Arch Virol"},{"key":"13902_CR42","doi-asserted-by":"publisher","first-page":"390","DOI":"10.1016\/j.virol.2008.03.023","volume":"376","author":"NL Forrester","year":"2008","unstructured":"Forrester, N. L., Moss, S. R., Turner, S. L., Schirrmeier, H. & Gould, E. A. Recombination in rabbit haemorrhagic disease virus: possible impact on evolution and epidemiology. Virology \n                           376, 390\u2013396, https:\/\/doi.org\/10.1016\/j.virol.2008.03.023 (2008).","journal-title":"Virology"},{"key":"13902_CR43","doi-asserted-by":"publisher","unstructured":"Hu, B. et al. Recombination between G2 and G6 strains of rabbit hemorrhagic disease virus (RHDV) in China. 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