Archives of Virology

, Volume 161, Issue 4, pp 811–820 | Cite as

Comparison of beak and feather disease virus prevalence and immunity-associated genetic diversity over time in an island population of red-crowned parakeets

  • Gabrielle J. KnaflerEmail author
  • Luis Ortiz-Catedral
  • Bethany Jackson
  • Arvind Varsani
  • Catherine E. Grueber
  • Bruce C. Robertson
  • Ian G. Jamieson
Original Article


Pathogen outbreaks in the wild can contribute to a population’s extinction risk. Concern over the effects of pathogen outbreaks in wildlife is amplified in small, threatened populations, where degradation of genetic diversity may hinder natural selection for enhanced immunocompetence. Beak and feather disease virus (BFDV) was detected for the first time in an island population of red-crowned parakeets (Cyanoramphus novaezelandiae) in 2008 on Little Barrier Island (Hauturu-o-Toi) of New Zealand. By 2013, the prevalence of the viral infection had significantly decreased within the population. We tested whether the population of red-crowned parakeets showed a selective response to BFDV, using neutral microsatellite and two immunity-associated genetic markers, the major histocompatibility complex (MHC) and Toll-like receptors (TLRs). We found evidence for selection at viral-associated TLR3; however, the ability of TLR3 to elicit an immune response in the presence of BFDV warrants confirmation. Alternatively, because red-crowned parakeet populations are prone to fluctuations in size, the decrease in BFDV prevalence over time may be attributed to the Little Barrier Island population dropping below the density threshold for viral maintenance. Our results highlight that natural processes such as adaptation for enhanced immunocompetence and/or density fluctuations are efficient mechanisms for reducing pathogen prevalence in a threatened, isolated population.


Major Histocompatibility Complex Major Histocompatibility Complex Class Major Histocompatibility Complex Allele Infinite Allele Model Genetic Diversity Pattern 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We are grateful to Gregory Gimenez, Les McNoe, and Monika Zavodna at Otago Genomics and Bioinformatics Facility for their valuable NGS advice. Capture and sampling of red-crowned parakeets was conducted under approved permits by the New Zealand Department of Conservation (permits AK-15300-RES, AK-20666-FAU, AK-22857-FAU). This research was supported by an Allan Wilson Centre grant to IGJ and University of Otago scholarship to GJK.

Supplementary material

705_2015_2717_MOESM1_ESM.docx (13 kb)
Supplementary material 1 (DOCX 12 kb)
705_2015_2717_MOESM2_ESM.docx (168 kb)
Supplementary material 2 (DOCX 168 kb)


  1. 1.
    O’Brien SJ, Evermann JF (1988) Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol 3:254–259CrossRefPubMedGoogle Scholar
  2. 2.
    de Castro F, Bolker B (2005) Mechanisms of disease-induced extinction. Ecol Lett 8:117–126CrossRefGoogle Scholar
  3. 3.
    Skerratt LF, Berger L, Speare R et al (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 4:125–134CrossRefGoogle Scholar
  4. 4.
    Heard MJ, Smith KF, Ripp KJ et al (2013) The threat of disease increases as species move toward extinction. Conserv Biol 27:1378–1388CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Lyles AM, Dobson AP (1993) Infectious disease and intensive management: population dynamics, threatened hosts, and their parasites. J Zoo Wild Med 24:315–326Google Scholar
  6. 6.
    Westerdahl H, Hansson B, Bensch S et al (2004) Between-year variation of MHC allele frequencies in great reed warblers: selection or drift? J Evol Biol 17:485–492CrossRefPubMedGoogle Scholar
  7. 7.
    Hawley DM, Fleischer RC (2012) Contrasting epidemic histories reveal pathogen-mediated balancing selection on class II MHC diversity in a wild songbird. PLoS One 7:e30222CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Spurgin LG, Richardson DS (2010) How pathogens drive genetic diversity: MHC, mechanisms and misunderstandings. Proc R Soc B Biol Sci 277:979–988CrossRefGoogle Scholar
  9. 9.
    Ortiz-Catedral L, McInnes K, Hauber ME et al (2009) First report of beak and feather disease virus (BFDV) in wild red-fronted parakeets (Cyanoramphus novaezelandiae) in New Zealand. Emu 109:244–247CrossRefGoogle Scholar
  10. 10.
    Massaro M, Ortiz-Catedral L, Julian L et al (2012) Molecular characterisation of beak and feather disease virus (BFDV) in New Zealand and its implications for managing an infectious disease. Arch Virol 157:1651–1663CrossRefPubMedGoogle Scholar
  11. 11.
    Pass DA, Perry RA (1984) The pathology of psittacine beak and feather disease. Aust Vet J 61:69–74CrossRefPubMedGoogle Scholar
  12. 12.
    Raidal SR (1995) Viral skin diseases of birds. Semin Avian Exot Pet Med Viral Dis 4:72–82CrossRefGoogle Scholar
  13. 13.
    Todd D (2000) Circoviruses: immunosuppressive threats to avian species: a review. Avian Pathol 29:373–394CrossRefPubMedGoogle Scholar
  14. 14.
    Ha HJ, Anderson IL, Alley MR et al (2007) The prevalence of beak and feather disease virus infection in wild populations of parrots and cockatoos in New Zealand. N Z Vet J 55:235–238CrossRefPubMedGoogle Scholar
  15. 15.
    Harkins GW, Martin DP, Christoffels A et al (2014) Towards inferring the global movement of beak and feather disease virus. Virology 450–451:24–33CrossRefPubMedGoogle Scholar
  16. 16.
    Jackson B, Varsani A, Holyoake C et al (2015) Emerging infectious disease or evidence of endemicity? A multi-season study of Beak and feather disease virus in wild Red-crowned Parakeets (Cyanoramphus novaezelandiae). Arch Virol. 160:2283–2292CrossRefPubMedGoogle Scholar
  17. 17.
    Ritchie BW, Niagro FD, Latimer KS et al (1991) Routes of prevalence of shedding of psittacine beak and feather disease virus. Am J Vet Res 52:1804–1809PubMedGoogle Scholar
  18. 18.
    Rahaus M, Desloges N, Probst S et al (2008) Detection of beak and feather disease virus DNA in embryonated eggs of psittacine birds. Vet Med 53:53–58Google Scholar
  19. 19.
    Jarne P, Lagoda PJ (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429CrossRefPubMedGoogle Scholar
  20. 20.
    Garstka MA, Fish A, Celie PHN et al (2015) The first step of peptide selection in antigen presentation by MHC class I molecules. Proc Natl Acad Sci USA 112:1505–1510CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Alcaide M, Edwards SV, Cadahía L et al (2009) MHC class I genes of birds of prey: isolation, polymorphism and diversifying selection. Conserv Genet 10:1349–1355CrossRefGoogle Scholar
  22. 22.
    Medzhitov R (2001) Toll-like receptors and innate immunity. Nat Rev Immunol 1:135–145CrossRefPubMedGoogle Scholar
  23. 23.
    Brownlie R, Allan B (2011) Avian toll-like receptors. Cell Tissue Res 343:121–130CrossRefPubMedGoogle Scholar
  24. 24.
    Ritchie BW, Niagro FD, Lukert PD et al (1989) Characterization of a new virus from cockatoos with psittacine beak and feather disease. Virology 171:83–88CrossRefPubMedGoogle Scholar
  25. 25.
    Ortiz-Catedral L, Brunton DH (2009) Nesting sites and nesting success of reintroduced red-crowned parakeets (Cyanoramphus novaezelandiae) on Tiritiri Matangi Island, New Zealand. N Z J Zool 35:1–10CrossRefGoogle Scholar
  26. 26.
    Ortiz-Catedral L, Hauber ME, Brunton DH (2013) Growth and survival of nestlings in a population of red-crowned parakeets (Cyanoramphus novaezelandiae) free of introduced mammalian nest predators on Tiritiri Matangi Island, New Zealand. N Z J Ecol 37:370–378Google Scholar
  27. 27.
    Taylor RH (1985) Status, habits and conservation of Cyanoramphus parakeets in the New Zealand region. ICBP Tech Publ 3:195–211Google Scholar
  28. 28.
    Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158CrossRefGoogle Scholar
  29. 29.
    Ortiz-Catedral L, Kurenbach B, Massaro M et al (2010) A new isolate of Beak and feather disease virus from endemic wild Red-fronted parakeets (Cyanoramphus novaezelandiae) in New Zealand. Arch Virol 155:613–620CrossRefPubMedGoogle Scholar
  30. 30.
    Chan C, Ballantyne KN, Lambert DM et al (2005) Characterization of variable microsatellite loci in Forbes’ parakeet (Cyanoramphus forbesi) and their use in other parrots. Conserv Genet 6:651–654CrossRefGoogle Scholar
  31. 31.
    Andrews BJ, Hale ML, Steeves TE (2012) Characterisation of microsatellite loci in the critically endangered orange-fronted kākāriki (Cyanoramphus malherbi) isolated using genomic next generation sequencing. Conserv Genet Resour 5:235–237CrossRefGoogle Scholar
  32. 32.
    Knafler GJ, Jamieson IG, Robertson BC (2014) Microsatellite primers for the red-crowned parakeet (Cyanoramphus novaezelandiae). Conserv Genet Resour 7:419–421CrossRefGoogle Scholar
  33. 33.
    Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234CrossRefPubMedGoogle Scholar
  34. 34.
    van Oosterhout C, Hutchinson WF, Wills DPM et al (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  35. 35.
    Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567CrossRefPubMedGoogle Scholar
  36. 36.
    Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  37. 37.
    R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing.
  38. 38.
    Lenz TL, Becker S (2008) Simple approach to reduce PCR artefact formation leads to reliable genotyping of MHC and other highly polymorphic loci-implications for evolutionary analysis. Gene 427:117–123CrossRefPubMedGoogle Scholar
  39. 39.
    Knafler GJ, Jamieson IG (2014) Primers for the amplification of major histocompatibility complex class I and II loci in the recovering red-crowned parakeet. Conserv Genet Resour 6:37–39CrossRefGoogle Scholar
  40. 40.
    Yuhki N, O’Brien SJ (1990) DNA variation of the mammalian major histocompatibility complex reflects genomic diversity and population history. Proc Natl Acad Sci USA 87:836–840CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nuc Acids Symp Ser 41:95–98Google Scholar
  42. 42.
    Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  43. 43.
    Tamura K, Dudley J, Nei M et al (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  44. 44.
    Kosakovsky Pond SL, Frost SDW, Muse SV (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics 21:676–679CrossRefGoogle Scholar
  45. 45.
    Delport W, Poon AFY, Frost SDW et al (2010) Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26:2455–2457CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Kosakovsky Pond SL, Posada D, Gravenor MB et al (2006) GARD: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098CrossRefPubMedGoogle Scholar
  47. 47.
    Kosakovsky Pond SL, Frost SDW (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222CrossRefPubMedGoogle Scholar
  48. 48.
    Sutton JT, Robertson BC, Grueber CE et al (2013) Characterization of MHC class II B polymorphism in bottlenecked New Zealand saddlebacks reveals low levels of genetic diversity. Immunogenetics 65:619–633CrossRefPubMedGoogle Scholar
  49. 49.
    Sandberg M, Eriksson L, Sjo M (1998) New chemical descriptors relevant for the design of biologically active peptides. A multivariate characterization of 87 amino acids. J Med Chem 2623:2481–2491CrossRefGoogle Scholar
  50. 50.
    Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405CrossRefPubMedGoogle Scholar
  51. 51.
    Sepil I, Moghadam HK, Huchard E et al (2012) Characterization and 454 pyrosequencing of major histocompatibility complex class I genes in the great tit reveal complexity in a passerine system. BMC Evol Biol 12:68CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Sutton JT, Robertson BC, Jamieson IG (2015) MHC variation reflects the bottleneck histories of New Zealand passerines. Mol Ecol 24:362–373CrossRefPubMedGoogle Scholar
  53. 53.
    Grueber CE, Jamieson IG (2013) Primers for amplification of innate immunity toll-like receptor loci in threatened birds of the Apterygiformes, Gruiformes, Psittaciformes and Passeriformes. Conserv Genet Resour 5:1043–1047CrossRefGoogle Scholar
  54. 54.
    Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Stephens M, Donnelly P (2003) A comparison of bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedPubMedCentralGoogle Scholar
  57. 57.
    Kundu S, Faulkes CG, Greenwood AG et al (2012) Tracking viral evolution during a disease outbreak: the rapid and complete selective sweep of a circovirus in the endangered Echo parakeet. J Virol 86:5221–5229CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Jackson B, Lorenzo A, Theuerkauf J et al (2014) Preliminary surveillance for beak and feather disease virus in wild parrots of New Caledonia: implications of a reservoir species for Ouvea Parakeets. Emu 114:283–289CrossRefGoogle Scholar
  59. 59.
    Peters A, Patterson EI, Baker BGB et al (2014) Evidence of psittacine beak and feather disease virus spillover into wild critically endangered orange-bellied parrots (Neophema chrysogaster). J Wildl Dis 50:288–296CrossRefPubMedGoogle Scholar
  60. 60.
    Sarker S, Ghorashi S, Forwood J et al (2014) Phylogeny of beak and feather disease virus in cockatoos demonstrates host generalism and multiple-variant infections within Psittaciformes. Virol 460:72–82CrossRefGoogle Scholar
  61. 61.
    Regnard G, Rutledge S, Martin R et al (2015) Beak and feather disease virus: correlation between viral load and clinical signs in wild Cape parrots (Poicephalus robustus) in South Africa. Arch Virol 160:339–344CrossRefPubMedGoogle Scholar
  62. 62.
    Wobeser G (2002) Disease management strategies for wildlife disease management—important concepts. Rev Sci Tech Off Int Epiz 21:159–178CrossRefGoogle Scholar
  63. 63.
    Shim E, Galvani AP (2009) Evolutionary repercussions of avian culling on host resistance and influenza virulence. PLoS One 4:e5508CrossRefGoogle Scholar
  64. 64.
    Lane-deGraaf KE, Amish SJ, Gardipee F et al (2014) Signatures of natural and unnatural selection: evidence from an immune system gene in African buffalo. Conserv Genet 16:289–300CrossRefGoogle Scholar
  65. 65.
    Miller HC, Allendorf F, Daugherty CH (2010) Genetic diversity and differentiation at MHC genes in island populations of tuatara (Sphenodon spp.). Mol Ecol 19:3894–3908CrossRefPubMedGoogle Scholar
  66. 66.
    Sutton JT, Nakagawa S, Robertson BC et al (2011) Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol 20:4408–4420CrossRefPubMedGoogle Scholar
  67. 67.
    Grueber CE, Knafler GJ, King TM et al (2015) Toll-like receptor diversity in 10 threatened bird species : relationship with microsatellite heterozygosity. Conserv Genet 16:595–611CrossRefGoogle Scholar
  68. 68.
    Greene TC (2013) Red-crowned parakeet. In: Miskelly CM (ed) New Zealand Birds Online.
  69. 69.
    Doherty PC, Zinkernagel RM (1975) Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex. Nature 256:50–52CrossRefPubMedGoogle Scholar
  70. 70.
    Takahata N, Nei M (1990) Allelic genealogy under over- dominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics 124:967–978PubMedPubMedCentralGoogle Scholar
  71. 71.
    Radwan J, Biedrzycka A, Babik W (2010) Does reduced MHC diversity decrease viability of vertebrate populations? Biol Conserv 143:537–544CrossRefGoogle Scholar
  72. 72.
    Strand TM, Segelbacher G, Quintela M et al (2012) Can balancing selection on MHC loci counteract genetic drift in small fragmented populations of black grouse? Ecol Evol 2:341–353CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Grueber CE, Wallis GP, Jamieson IG (2013) Genetic drift outweighs natural selection at toll-like receptor (TLR) immunity loci in a re-introduced population of a threatened species. Mol Ecol 22:4470–4482CrossRefPubMedGoogle Scholar
  74. 74.
    Aguilar A, Roemer G, Debenham S et al (2004) High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc Natl Acad Sci USA 101:3490–3494CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    van Oosterhout C, Joyce DA, Cummings SM et al (2006) Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulate). Evolution 60:2562–2574CrossRefPubMedGoogle Scholar
  76. 76.
    Abdul-Careem MF, Haq K, Shanmuganathan S et al (2009) Induction of innate host responses in the lungs of chickens following infection with a very virulent strain of Marek’s disease virus. Virology 393:250–257CrossRefPubMedGoogle Scholar
  77. 77.
    Wagner H, Bauer S (2006) All is not Toll: new pathways in DNA recognition. J Exp Med 203:265–268CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Altschul S, Gish W, Miller W (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  79. 79.
    Raidal SR, Cross GM (1995) Acute necrotizing hepatitis caused by experimental infection with psittacine beak and feather disease virus. J Avian Med Surg 9:36–40Google Scholar
  80. 80.
    Schoemaker NJ, Dorrestein GM, Latimer KS et al (2000) Severe leukopenia and liver necrosis in young African Grey Parrots (Psittacus erithacus erithacus) infected with psittacine circovirus. Avian Dis 44:470–478CrossRefPubMedGoogle Scholar
  81. 81.
    Doneley RJT (2003) Acute beak and feather disease in juvenile African Grey parrots—an uncommon presentation of a common disease. Aust Vet J 81:206–207CrossRefPubMedGoogle Scholar
  82. 82.
    Robino P, Grego E, Rossi G et al (2014) Molecular analysis and associated pathology of beak and feather disease virus isolated in Italy from young Congo African grey parrots (Psittacus erithacus) with an “atypical peracute form” of the disease. Avian Pathol 43:333–344CrossRefPubMedGoogle Scholar
  83. 83.
    Fellah JS, Jaffredo T, Dunon D (2008) Development of the avian immune system. Avian Immunol 4:51–66CrossRefGoogle Scholar
  84. 84.
    Lloyd-Smith JO, Cross PC, Briggs CJ et al (2005) Should we expect population thresholds for wildlife disease? Trends Ecol Evol 20:511–519CrossRefPubMedGoogle Scholar
  85. 85.
    Elliott GP, Dilks PJ, O’Donnell CFJ (1996) The ecology of yellow-crowned parakeets (Cyanoramphus auriceps) in Nothofagus forest in Fiordland, New Zealand. New Zeal J Zool 23:249–265CrossRefGoogle Scholar
  86. 86.
    Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Gabrielle J. Knafler
    • 1
    Email author
  • Luis Ortiz-Catedral
    • 2
  • Bethany Jackson
    • 3
  • Arvind Varsani
    • 4
    • 5
    • 6
  • Catherine E. Grueber
    • 1
    • 7
    • 8
  • Bruce C. Robertson
    • 1
  • Ian G. Jamieson
    • 1
  1. 1.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  2. 2.Ecology and Conservation Group, Institute of Natural and Mathematical SciencesMassey UniversityAucklandNew Zealand
  3. 3.College of Veterinary MedicineMurdoch UniversityPerthAustralia
  4. 4.Centre for Integrative Ecology, Biomolecular Interaction Centre and School of Biological SciencesUniversity of CanterburyChristchurchNew Zealand
  5. 5.Structural Biology Research Unit, Division of Medical Biochemistry, Department of Clinical Laboratory SciencesUniversity of Cape TownCape TownSouth Africa
  6. 6.Department of Plant Pathology and Emerging Pathogens InstituteUniversity of FloridaGainesvilleUSA
  7. 7.Faculty of Veterinary ScienceUniversity of SydneySydneyAustralia
  8. 8.San Diego Zoo GlobalSan DiegoUSA

Personalised recommendations