Skip to content
1887

Abstract

Polyomaviruses and papillomaviruses are icosahedral viruses with small circular dsDNA genomes. Limited information on their diversity and evolution in avian hosts is available, with even less known regarding Antarctic penguins. Prior to this study, only one polyomavirus and two papillomaviruses had been identified in Adélie penguins (). To expand our knowledge of these viruses in Antarctic penguins, we collected faecal and cloacal swab samples from 246 Adélie penguins over 3 breeding seasons (2021–2024) and 10 emperor penguins () during the 2023–2024 season on Ross Island (Ross Sea). Additionally, we sampled 66 Adélie, 40 chinstrap () and 71 gentoo () penguins during the 2022–2023 season across various sites on the Antarctic Peninsula. All samples were screened for papillomaviruses and polyomaviruses. We identified 31 polyomaviruses in Adélie, gentoo and chinstrap penguins and 4 papillomaviruses in Adélie penguins sampled in both eastern and western Antarctica. The 31 penguin polyomaviruses belong to a single species but form four distinct variants that are host species specific with strong geographic clustering. The four papillomaviruses represent three different types, of which two are new types from Adélie penguins sampled on Yalour Island in the West Antarctic Peninsula. Co-occurrence of two polyomavirus variants was identified in two individual gentoo penguins. Both of these variants appear to be circulating in gentoo penguins at Cierva Cove, Hope Bay in Trinity Peninsula along the Antarctic Peninsula, and at Hannah Point on Livingstone Island and Stranger Point on King George Island in the South Shetland Islands. Here, we expand the known diversity, host and geographical ranges of penguin polyomaviruses and, together with a previously identified polyomavirus on Ross Island from 2012 to 2013, show that they form five distinct lineages. The four papillomaviruses identified in this study, together with two previously identified from Ross Island in 2012 and 2013 breeding seasons, show substantial diversity reflecting four papillomavirus types across three viral species and two distinct genera. Continued surveillance and viral genomic analysis across a larger geographical framework will help understand the evolution, transmission and incidence rates of these viruses.

Funding
This study was supported by the:
  • Ministerio de Economía y Competitividad (Award PID2019-108597RB-I00)
    • Principal Award Recipient: NotApplicable
  • National Science Foundation (Award 1935870)
    • Principal Award Recipient: NotApplicable
  • National Science Foundation (Award 2040199)
    • Principal Award Recipient: NotApplicable
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001580
2025-11-24
2025-12-16

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/mgen/11/11/mgen001580.html?itemId=/content/journal/mgen/10.1099/mgen.0.001580&mimeType=html&fmt=ahah

References

  1. Kooyman GL. Evolutionary and ecological aspects of some Antarctic and sub-Antarctic penguin distributions. Oecologia 2002; 130:485–495 [View Article] [PubMed]
    [Google Scholar]
  2. Ainley DG, Wilson RP. The Aquatic World of Penguins: Biology of Fish-Birds Springer; 2023
    [Google Scholar]
  3. Borboroglu PG, Boersma PD. Penguins: Natural History and Conservation University of Washington Press; 2015
    [Google Scholar]
  4. Smeele ZE, Ainley DG, Varsani A. Viruses associated with Antarctic wildlife: from serology based detection to identification of genomes using high throughput sequencing. Virus Res 2018; 243:91–105 [View Article] [PubMed]
    [Google Scholar]
  5. Lee S-Y, Kim J-H, Park YM, Shin OS, Kim H et al. A novel adenovirus in Chinstrap penguins (Pygoscelis antarctica) in Antarctica. Viruses 2014; 6:2052–2061 [View Article] [PubMed]
    [Google Scholar]
  6. Lee S-Y, Kim J-H, Seo T-K, No JS, Kim H et al. Genetic and molecular epidemiological characterization of a novel adenovirus in Antarctic penguins collected between 2008 and 2013. PLoS One 2016; 11:e0157032 [View Article]
    [Google Scholar]
  7. Grimaldi WW, Hall RJ, White DD, Wang J, Massaro M et al. First report of a feather loss condition in Adélie penguins (Pygoscelis adeliae) on Ross Island, Antarctica, and a preliminary investigation of its cause. Emu Austr Ornithol 2015; 115:185–189 [View Article]
    [Google Scholar]
  8. Wille M, Harvey E, Shi M, Gonzalez-Acuña D, Holmes EC et al. Sustained RNA virome diversity in Antarctic penguins and their ticks. ISME J 2020; 14:1768–1782 [View Article] [PubMed]
    [Google Scholar]
  9. Miller PJ, Afonso CL, Spackman E, Scott MA, Pedersen JC et al. Evidence for a new avian paramyxovirus serotype 10 detected in rockhopper penguins from the Falkland Islands. J Virol 2010; 84:11496–11504 [View Article] [PubMed]
    [Google Scholar]
  10. Neira V, Tapia R, Verdugo C, Barriga G, Mor S et al. Novel avulaviruses in penguins, Antarctica. Emerg Infect Dis 2017; 23:1212–1214 [View Article] [PubMed]
    [Google Scholar]
  11. Thomazelli LM, Araujo J, Oliveira DB, Sanfilippo L, Ferreira CS et al. Newcastle disease virus in penguins from King George Island on the Antarctic region. Vet Microbiol 2010; 146:155–160 [View Article] [PubMed]
    [Google Scholar]
  12. Levy H, Fiddaman SR, Djurhuus A, Black CE, Kraberger S et al. Identification of circovirus genome in a Chinstrap penguin (Pygoscelis antarcticus) and Adélie penguin (Pygoscelis adeliae) on the Antarctic Peninsula. Viruses 2002; 12:858 [View Article]
    [Google Scholar]
  13. Morandini V, Dugger KM, Ballard G, Elrod M, Schmidt A et al. Identification of a novel Adélie penguin circovirus at Cape Crozier (Ross Island, Antarctica). Viruses 2019; 11:1088 [View Article] [PubMed]
    [Google Scholar]
  14. Barriga GP, Boric-Bargetto D, San Martin MC, Neira V, van Bakel H et al. Avian influenza virus H5 strain with North American and Eurasian lineage genes in an Antarctic penguin. Emerg Infect Dis 2016; 22:2221–2223 [View Article] [PubMed]
    [Google Scholar]
  15. de Seixas MMM, de Araújo J, Krauss S, Fabrizio T, Walker D et al. H6N8 avian influenza virus in Antarctic seabirds demonstrates connectivity between South America and Antarctica. Transbound Emerg Dis 2022; 69:e3436–e3446 [View Article] [PubMed]
    [Google Scholar]
  16. Hurt AC, Vijaykrishna D, Butler J, Baas C, Maurer-Stroh S et al. Detection of evolutionarily distinct avian influenza A viruses in Antarctica. mBio 2014; 5:e01098–14 [View Article] [PubMed]
    [Google Scholar]
  17. Van Doorslaer K, Ruoppolo V, Schmidt A, Lescroël A, Jongsomjit D et al. Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins. Virus Evol 2017; 3:vex027 [View Article] [PubMed]
    [Google Scholar]
  18. Varsani A, Kraberger S, Jennings S, Porzig EL, Julian L et al. A novel papillomavirus in Adélie penguin (Pygoscelis adeliae) faeces sampled at the Cape Crozier colony, Antarctica. J Gen Virol 2014; 95:1352–1365 [View Article] [PubMed]
    [Google Scholar]
  19. Aasdev A, Mishra A, Nair M, Pawar SD, Dubey CK et al. Three complete genome sequences of penguin megrivirus from ornithogenic soil, Adélie penguin, and Weddell seal of Antarctica. Microbiology 2019 [View Article]
    [Google Scholar]
  20. de Souza WM, Fumagalli MJ, Martin MC, de Araujo J, Orsi MA et al. Pingu virus: a new picornavirus in penguins from Antarctica. Virus Evol 2019; 5:vez047 [View Article] [PubMed]
    [Google Scholar]
  21. Yinda CK, Esefeld J, Peter HU, Matthijnssens J, Zell R. Penguin megrivirus, a novel picornavirus from an Adélie penguin (Pygoscelis adeliae). Arch Virol 2019; 164:2887–2890 [View Article] [PubMed]
    [Google Scholar]
  22. Varsani A, Porzig EL, Jennings S, Kraberger S, Farkas K et al. Identification of an avian polyomavirus associated with Adélie penguins (Pygoscelis adeliae). J Gen Virol 2015; 96:851–857 [View Article] [PubMed]
    [Google Scholar]
  23. Levy H, Fontenele RS, Harding C, Suazo C, Kraberger S et al. Identification and distribution of novel cressdnaviruses and circular molecules in four penguin species in South Georgia and the Antarctic Peninsula. Viruses 2020; 12:1029 [View Article] [PubMed]
    [Google Scholar]
  24. Brister JR, Ako-Adjei D, Bao Y, Blinkova O. NCBI viral genomes resource. Nucleic Acids Res 2015; 43:D571–7 [View Article] [PubMed]
    [Google Scholar]
  25. Maclachlan NJ, Dubovi EJ. Fenner’s Veterinary Virology Academic press; 2010
    [Google Scholar]
  26. Thomas NJ, Hunter DB, Atkinson CT. Infectious Diseases of Wild Birds John Wiley & Sons; 2008 [View Article]
    [Google Scholar]
  27. Moens U, Calvignac-Spencer S, Lauber C, Ramqvist T, Feltkamp MCW et al. ICTV virus taxonomy profile: Polyomaviridae. J Gen Virol 2017; 98:1159–1160 [View Article]
    [Google Scholar]
  28. Van Doorslaer K, Chen Z, Bernard H-U, Chan PKS, DeSalle R et al. ICTV virus taxonomy profile: Papillomaviridae. J Gen Virol 2018; 99:989–990 [View Article]
    [Google Scholar]
  29. Koonin EV, Dolja VV, Krupovic M, Varsani A, Wolf YI et al. Global organization and proposed megataxonomy of the virus world. Microbiol Mol Biol Rev 2020; 84:e00061-19 [View Article] [PubMed]
    [Google Scholar]
  30. Buck CB, Van Doorslaer K, Peretti A, Geoghegan EM, Tisza MJ et al. The ancient evolutionary history of polyomaviruses. PLoS Pathog 2016; 12:e1005574 [View Article] [PubMed]
    [Google Scholar]
  31. Ehlers B, Anoh AE, Ben Salem N, Broll S, Couacy-Hymann E et al. Novel polyomaviruses in mammals from multiple orders and reassessment of polyomavirus evolution and taxonomy. Viruses 2019; 11:930 [View Article] [PubMed]
    [Google Scholar]
  32. Van Doorslaer K. Evolution of the Papillomaviridae. Virology 2013; 445:11–20 [View Article] [PubMed]
    [Google Scholar]
  33. Willemsen A, Bravo IG. Origin and evolution of papillomavirus (onco)genes and genomes. Philos Trans R Soc Lond B Biol Sci 2019; 374:20180303 [View Article] [PubMed]
    [Google Scholar]
  34. Bernard HU. Coevolution of papillomaviruses with human populations. Trends Microbiol 1994; 2:140–143 [View Article] [PubMed]
    [Google Scholar]
  35. King K, Larsen BB, Gryseels S, Richet C, Kraberger S et al. Coevolutionary analysis implicates toll-like receptor 9 in papillomavirus restriction. mBio 2022; 13:e0005422 [View Article] [PubMed]
    [Google Scholar]
  36. Torres C. Evolution and molecular epidemiology of polyomaviruses. Infect Genet Evol 2020; 79:104150 [View Article] [PubMed]
    [Google Scholar]
  37. Forni D, Cagliani R, Clerici M, Pozzoli U, Sironi M. You will never walk alone: codispersal of JC polyomavirus with human populations. Mol Biol Evol 2020; 37:442–454 [View Article] [PubMed]
    [Google Scholar]
  38. Kaszab E, Marton S, Dán Á, Farsang A, Bálint Á et al. Molecular epidemiology and phylodynamics of goose haemorrhagic polyomavirus. Transbound Emerg Dis 2020; 67:2602–2608 [View Article] [PubMed]
    [Google Scholar]
  39. Chen Z, DeSalle R, Schiffman M, Herrero R, Burk RD. Evolutionary dynamics of variant genomes of human papillomavirus types 18, 45, and 97. J Virol 2009; 83:1443–1455 [View Article] [PubMed]
    [Google Scholar]
  40. Rector A, Lemey P, Tachezy R, Mostmans S, Ghim S-J et al. Ancient papillomavirus-host co-speciation in Felidae. Genome Biol 2007; 8:R57 [View Article] [PubMed]
    [Google Scholar]
  41. Van Doorslaer K, Burk RD. Evolution of human papillomavirus carcinogenicity. Adv Virus Res 2010; 77:41–62 [View Article] [PubMed]
    [Google Scholar]
  42. Zehender G, Frati ER, Martinelli M, Bianchi S, Amendola A et al. Dating the origin and dispersal of human papillomavirus type 16 on the basis of ancestral human migrations. Infect Genet Evol 2016; 39:258–264 [View Article] [PubMed]
    [Google Scholar]
  43. Ong CK, Chan SY, Campo MS, Fujinaga K, Mavromara-Nazos P et al. Evolution of human papillomavirus type 18: an ancient phylogenetic root in Africa and intratype diversity reflect coevolution with human ethnic groups. J Virol 1993; 67:6424–6431 [View Article] [PubMed]
    [Google Scholar]
  44. Duffy S, Shackelton LA, Holmes EC. Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 2008; 9:267–276 [View Article] [PubMed]
    [Google Scholar]
  45. Dill JA, Ng TFF, Camus AC. Complete sequence of the smallest polyomavirus genome, giant guitarfish (Rhynchobatus djiddensis) polyomavirus 1. Genome Announc 2016; 4:e00391-16 [View Article] [PubMed]
    [Google Scholar]
  46. Peretti A, FitzGerald PC, Bliskovsky V, Pastrana DV, Buck CB. Genome sequence of a fish-associated polyomavirus, black sea bass (Centropristis striata) polyomavirus 1. Genome Announc 2015; 3:e01476-14 [View Article] [PubMed]
    [Google Scholar]
  47. Dela Cruz FN Jr, Li L, Delwart E, Pesavento PA. A novel pulmonary polyomavirus in alpacas (Vicugna pacos). Vet Microbiol 2017; 201:49–55 [View Article] [PubMed]
    [Google Scholar]
  48. Vargas KL, Kraberger S, Custer JM, Paietta EN, Culver M et al. Identification of a novel polyomavirus in wild Sonoran Desert rodents of the family Heteromyidae. Arch Virol 2023; 168:253 [View Article] [PubMed]
    [Google Scholar]
  49. Varsani A, Frankfurter G, Stainton D, Male MF, Kraberger S et al. Identification of a polyomavirus in Weddell seal (Leptonychotes weddellii) from the Ross Sea (Antarctica). Arch Virol 2017; 162:1403–1407 [View Article] [PubMed]
    [Google Scholar]
  50. Johne R, Müller H. Polyomaviruses of birds: etiologic agents of inflammatory diseases in a tumor virus family. J Virol 2007; 81:11554–11559 [View Article] [PubMed]
    [Google Scholar]
  51. Rott O, Kröger M, Müller H, Hobom G. The genome of budgerigar fledgling disease virus, an avian polyomavirus. Virology 1988; 165:74–86 [View Article] [PubMed]
    [Google Scholar]
  52. Abrantes J, Varsani A, Pereira P, Maia C, Farias I et al. Identification and characterization of a polyomavirus in the thornback skate (Raja clavata). Virol J 2023; 20:190 [View Article] [PubMed]
    [Google Scholar]
  53. López-Bueno A, Mavian C, Labella AM, Castro D, Borrego JJ et al. Concurrence of iridovirus, polyomavirus, and a unique member of a new group of fish papillomaviruses in lymphocystis disease-affected gilthead sea bream. J Virol 2016; 90:8768–8779 [View Article] [PubMed]
    [Google Scholar]
  54. Van Doorslaer K, Kraberger S, Austin C, Farkas K, Bergeman M et al. Fish polyomaviruses belong to two distinct evolutionary lineages. J Gen Virol 2018; 99:567–573 [View Article] [PubMed]
    [Google Scholar]
  55. Schmidlin K, Kraberger S, Cook C, DeNardo DF, Fontenele RS et al. A novel lineage of polyomaviruses identified in bark scorpions. Virology 2021; 563:58–63 [View Article] [PubMed]
    [Google Scholar]
  56. Guerin JL, Gelfi J, Dubois L, Vuillaume A, Boucraut-Baralon C et al. A novel polyomavirus (goose hemorrhagic polyomavirus) is the agent of hemorrhagic nephritis enteritis of geese. J Virol 2000; 74:4523–4529 [View Article] [PubMed]
    [Google Scholar]
  57. Halami MY, Dorrestein GM, Couteel P, Heckel G, Müller H et al. Whole-genome characterization of a novel polyomavirus detected in fatally diseased canary birds. J Gen Virol 2010; 91:3016–3022 [View Article] [PubMed]
    [Google Scholar]
  58. Krautwald ME, Müller H, Kaleta EF. Polyomavirus infection in budgerigars (Melopsittacus undulatus): clinical and aetiological studies. Zentralbl Veterinarmed B 1989; 36:459–467 [View Article] [PubMed]
    [Google Scholar]
  59. Wittig W, Hoffmann K, Müller H, Johne R. Detection of DNA of the finch polyomavirus in diseases of various types of birds in the order Passeriformes. Berl Munch Tierarztl Wochenschr 2007; 120:113–119 [PubMed]
    [Google Scholar]
  60. Pingret J-L, Boucraut-Baralon C, Guérin J-L. Goose haemorrhagic polyomavirus infection in ducks. Vet Rec 2008; 162:164 [View Article] [PubMed]
    [Google Scholar]
  61. Tu Y-C, Li W-T, Lee F, Huang C-W, Chang J-C et al. Localization of goose haemorrhagic polyomavirus in naturally infected geese using in situ hybridization. Avian Pathol 2021; 50:41–51 [View Article] [PubMed]
    [Google Scholar]
  62. Kraberger S, Austin C, Farkas K, Desvignes T, Postlethwait JH et al. Discovery of novel fish papillomaviruses: from the Antarctic to the commercial fish market. Virology 2022; 565:65–72 [View Article]
    [Google Scholar]
  63. Cardone G, Moyer AL, Cheng N, Thompson CD, Dvoretzky I et al. Maturation of the human papillomavirus 16 capsid. mBio 2014; 5:e01104–01114 [View Article]
    [Google Scholar]
  64. Van Doorslaer K, Li Z, Xirasagar S, Maes P, Kaminsky D et al. The papillomavirus episteme: a major update to the papillomavirus sequence database. Nucleic Acids Res 2017; 45:D499–D506 [View Article] [PubMed]
    [Google Scholar]
  65. Regney M, Kraberger S, Custer JM, Crane AE, Shero MR et al. Diverse papillomaviruses identified from Antarctic fur seals, leopard seals and Weddell seals from the Antarctic. Virology 2024; 594:110064 [View Article]
    [Google Scholar]
  66. Smeele ZE, Burns JM, Van Doorsaler K, Fontenele RS, Waits K et al. Diverse papillomaviruses identified in Weddell seals. J Gen Virol 2018; 99:549–557 [View Article] [PubMed]
    [Google Scholar]
  67. Pereson MJ, Sanabria DJ, Torres C, Liotta DJ, Campos RH et al. Evolutionary analysis of JC polyomavirus in Misiones’ population yields insight into the population dynamics of the early human dispersal in the Americas. Virology 2023; 585:100–108 [View Article] [PubMed]
    [Google Scholar]
  68. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30:2114–2120 [View Article]
    [Google Scholar]
  69. Li D, Luo R, Liu C-M, Leung C-M, Ting H-F et al. MEGAHIT v1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 2016; 102:3–11 [View Article]
    [Google Scholar]
  70. Buchfink B, Reuter K, Drost HG. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods 2021; 18:366–368 [View Article] [PubMed]
    [Google Scholar]
  71. Aroney STN, Newell RJP, Nissen JN, Camargo AP, Tyson GW et al. CoverM: read alignment statistics for metagenomics. Bioinformatics 2025; 41:btaf147 [View Article] [PubMed]
    [Google Scholar]
  72. Muhire BM, Varsani A, Martin DP. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 2014; 9:e108277 [View Article]
    [Google Scholar]
  73. Crooks GE, Hon G, Chandonia JM, Brenner SE. WebLogo: a sequence logo generator. Genome Res 2004; 14:1188–1190 [View Article] [PubMed]
    [Google Scholar]
  74. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article] [PubMed]
    [Google Scholar]
  75. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article]
    [Google Scholar]
  76. Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 2017; 14:587–589 [View Article] [PubMed]
    [Google Scholar]
  77. Stöver BC, Müller KF. TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 2010; 11:7 [View Article]
    [Google Scholar]
  78. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics (Oxford, England) 2009; 25:1972–1973 [View Article] [PubMed]
    [Google Scholar]
  79. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011; 27:1164–1165 [View Article] [PubMed]
    [Google Scholar]
  80. Agius JE, Phalen DN, Rose K, Eden JS. New insights into Sauropsid Papillomaviridae evolution and epizootiology: discovery of two novel papillomaviruses in native and invasive island geckos. Virus Evol 2019; 5:vez051 [View Article]
    [Google Scholar]
  81. Martin DP, Varsani A, Roumagnac P, Botha G, Maslamoney S et al. RDP5: a computer program for analyzing recombination in, and removing signals of recombination from, nucleotide sequence datasets. Virus Evol 2021; 7:veaa087 [View Article]
    [Google Scholar]
  82. DeCaprio JA, Garcea RL. A cornucopia of human polyomaviruses. Nat Rev Microbiol 2013; 11:264–276 [View Article]
    [Google Scholar]
  83. An P, Sáenz Robles MT, Pipas JM. Large T antigens of polyomaviruses: amazing molecular machines. Annu Rev Microbiol 2012; 66:213–236 [View Article] [PubMed]
    [Google Scholar]
  84. Li D, Zhao R, Lilyestrom W, Gai D, Zhang R et al. Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature 2003; 423:512–518 [View Article]
    [Google Scholar]
  85. Pertierra LR, Segovia NI, Noll D, Martinez PA, Pliscoff P et al. Cryptic speciation in gentoo penguins is driven by geographic isolation and regional marine conditions: unforeseen vulnerabilities to global change. Diversity and Distributions 2020; 26:958–975 [View Article]
    [Google Scholar]
  86. Bernier G, Morin M, Marsolais G. A generalized inclusion body disease in the budgerigar (Melopsittacus undulatus) caused by a papovavirus-like agent. Avian Dis 1981; 25:1083–1092 [View Article] [PubMed]
    [Google Scholar]
  87. Davis RB, Bozeman LH, Gaudry D, Fletcher OJ, Lukert PD et al. A viral disease of fledgling budgerigars. Avian Dis 1981; 25:179–183 [View Article] [PubMed]
    [Google Scholar]
  88. Adiguzel MC, Timurkan MO, Cengiz S. Investigation and sequence analysis of avian polyomavirus and psittacine beak and feather disease virus from companion birds in Eastern Turkey. J Vet Res 2020; 64:495–501 [View Article] [PubMed]
    [Google Scholar]
  89. Bert E, Tomassone L, Peccati C, Navarrete MG, Sola SC. Detection of beak and feather disease virus (BFDV) and avian polyomavirus (APV) DNA in psittacine birds in Italy. J Vet Med B Infect Dis Vet Public Health 2005; 52:64–68 [View Article]
    [Google Scholar]
  90. Dolz G, Sheleby-Elías J, Romero-Zuñiga JJ, Vargas-Leitón B, Gutiérrez-Espeleta G et al. Prevalence of psittacine beak and feather disease virus and avian polyomavirus in captivity psittacines from Costa Rica. OJVM 2013; 03:240–245 [View Article]
    [Google Scholar]
  91. González-Hein G, Gil IA, Sanchez R, Huaracan B. Prevalence of avian polyomavirus 1 and beak and feather disease virus in exotic captive psittacine birds in Chile. J Avian Med Surg 2019; 33:141–149 [View Article] [PubMed]
    [Google Scholar]
  92. Hsu CM, Ko CY, Tsaia HJ. Detection and sequence analysis of avian polyomavirus and psittacine beak and feather disease virus from psittacine birds in Taiwan. Avian Dis 2006; 50:348–353 [View Article] [PubMed]
    [Google Scholar]
  93. Khosravi M, Samakkhah SA, Khoshbakht R, Mamouri KS. Avian polyomavirus among psittacine birds in iran: molecular detection rate and associated risk factors. J Avian Med Surg 2024; 38:7–14 [View Article] [PubMed]
    [Google Scholar]
  94. Philadelpho NA, Chacón RD, Diaz Forero AJ, Guimarães MB, Astolfi-Ferreira CS et al. Detection of aves polyomavirus 1 (APyV) and beak and feather disease virus (BFDV) in exotic and native Brazilian Psittaciformes. Braz J Microbiol 2022; 53:1665–1673 [View Article] [PubMed]
    [Google Scholar]
  95. Wan C, Chen C, Cheng L, Liu R, Fu G et al. Genomic analysis of Sheldrake origin goose hemorrhagic polyomavirus, China. J Vet Sci 2018; 19:782–787 [View Article] [PubMed]
    [Google Scholar]
  96. Siedlecka M, Chmielewska-Władyka M, Kublicka A, Wieliczko A, Matczuk AK. Goose parvovirus, goose hemorrhagic polyomavirus and goose circovirus infections are prevalent in commercial geese flocks in Poland and contribute to overall health and production outcomes: a two-year observational study. BMC Vet Res 2025; 21:216 [View Article] [PubMed]
    [Google Scholar]
  97. Phalen DN, Wilson VG, Graham DL. Organ distribution of avian polyomavirus DNA and virus-neutralizing antibody titers in healthy adult budgerigars. Am J Vet Res 1993; 54:2040–2047 [PubMed]
    [Google Scholar]
  98. Ehlers B, Moens U. Genome analysis of non-human primate polyomaviruses. Infect Genet Evol 2014; 26:283–294 [View Article] [PubMed]
    [Google Scholar]
  99. Canuti M, Munro HJ, Robertson GJ, Kroyer ANK, Roul S et al. New insight into avian papillomavirus ecology and evolution from characterization of novel wild bird papillomaviruse. Front Microbiol 2019; 10:701 [View Article] [PubMed]
    [Google Scholar]
  100. Bergvall M, Melendy T, Archambault J. The E1 proteins. Virology 2013; 445:35–56
    [Google Scholar]
  101. McBride AA. The papillomavirus E2 proteins. Virology 2013; 445:57–79 [View Article]
    [Google Scholar]
  102. Buck CB, Day PM, Trus BL. The papillomavirus major capsid protein L1. Virology 2013; 445:169–174 [View Article] [PubMed]
    [Google Scholar]
  103. Wang JW, Roden RBS. L2, the minor capsid protein of papillomavirus. Virology 2013; 445:175–186 [View Article]
    [Google Scholar]
  104. Gaynor AM, Fish S, Duerr RS, Cruz FND Jr, Pesavento PA. Identification of a novel papillomavirus in a northern fulmar (Fulmarus glacialis) with viral production in cartilage. Vet Pathol 2015; 52:553–561 [View Article] [PubMed]
    [Google Scholar]
  105. Rosenbaum CS, Wünschmann A, Armién AG, Schott R, Singh VK et al. Novel papillomavirus in a mallard duck with mesenchymal chondroid dermal tumors. J Vet Diagn Invest 2022; 34:231–236 [View Article] [PubMed]
    [Google Scholar]
  106. Roman A, Munger K. The papillomavirus E7 proteins. Virology 2013; 445:138–168 [View Article] [PubMed]
    [Google Scholar]
  107. Vande Pol SB, Klingelhutz AJ. Papillomavirus E6 oncoproteins. Virology 2013; 445:115–137 [View Article] [PubMed]
    [Google Scholar]
  108. Van Doorslaer K, Ould M’hamed Ould Sidi A, Zanier K, Rybin V, Deryckère F et al. Identification of unusual E6 and E7 proteins within avian papillomaviruses: cellular localization, biophysical characterization, and phylogenetic analysis. J Virol 2009; 83:8759–8770 [View Article]
    [Google Scholar]
  109. Giarrè M, Caldeira S, Malanchi I, Ciccolini F, Leão MJ et al. Induction of pRb degradation by the human papillomavirus type 16 E7 protein is essential to efficiently overcome p16INK4a-imposed G1 cell cycle arrest. J Virol 2001; 75:4705–4712 [View Article] [PubMed]
    [Google Scholar]
  110. Nominé Y, Masson M, Charbonnier S, Zanier K, Ristriani T et al. Structural and functional analysis of E6 oncoprotein: insights in the molecular pathways of human papillomavirus-mediated pathogenesis. Molecular Cell 2006; 21:665–678 [View Article]
    [Google Scholar]
  111. Dugger KM, Ainley DG, Lyver PO, Barton K, Ballard G. Survival differences and the effect of environmental instability on breeding dispersal in an Adélie penguin meta-population. Proc Natl Acad Sci USA 2010; 107:12375–12380 [View Article]
    [Google Scholar]
  112. Shepherd LD, Millar CD, Ballard G, Ainley DG, Wilson PR et al. Microevolution and mega-icebergs in the Antarctic. Proc Natl Acad Sci USA 2005; 102:16717–16722 [View Article]
    [Google Scholar]
  113. Lynch HJ, LaRue MA. First global census of the Adélie Penguin. The Auk 2014; 131:457–466 [View Article]
    [Google Scholar]
  114. Santora JA, LaRue MA, Ainley DG. Geographic structuring of Antarctic penguin populations. Global Ecol Biogeogr 2020; 29:1716–1728 [View Article]
    [Google Scholar]
  115. Woehler EJ, Poncet S. International Council of Scientific UnionsScientific Committee on Antarctic R The Distribution and Abundance of Antarctic and Subantarctic Penguins Scientific Committee on Antarctic Research (SCAR); 1993
    [Google Scholar]
  116. Jongsomjit D, Lescroël A, Schmidt AE, Lisovski S, Ainley DG et al. Going with the floe: sea-ice movement affects distance and destination during Adélie penguin winter movements. Ecology 2024; 105:e4196 [View Article] [PubMed]
    [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001580
Loading
/content/journal/mgen/10.1099/mgen.0.001580
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error